Next Article in Journal
Effect of the Sterile Insect Technique and Augmentative Parasitoid Releases in a Fruit Fly Suppression Program in Mango-Producing Areas of Southeast Mexico
Previous Article in Journal
Ecological Interactions of Predatory Mites, Cheyletus eruditus (Schrank) (Trombidiformes: Cheyletidae) and Cheyletus malaccensis Oudemans, and Prey, Liposcelis decolor (Pearman) (Psocodea: Liposcelididae), under Different Thermo-Hygrometric Regimes
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 14
Issue 9
10.3390/insects14090718
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Biotechnological Potential of Microorganisms for Mosquito Population Control and Reduction in Vector Competence

by
Ricardo de Melo Katak
1,
Amanda Montezano Cintra
2,
Bianca Correa Burini
3,
Osvaldo Marinotti
4,
Jayme A. Souza-Neto
2,† and
Elerson Matos Rocha
2,*
1
Malaria and Dengue Laboratory, Instituto Nacional de Pesquisas da Amazônia-INPA, Manaus 69060-001, AM, Brazil
2
Multiuser Central Laboratory, Department of Bioprocesses and Biotechnology, School of Agricultural Sciences, São Paulo State University (UNESP), Botucatu 18610-034, SP, Brazil
3
Florida Medical Entomology Laboratory, University of Florida, Vero Beach, FL 32962, USA
4
Department of Biology, Indiana University, Bloomington, IN 47405, USA
*
Author to whom correspondence should be addressed.
†
Current address: Department of Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, KS 66506, USA.
Insects 2023, 14(9), 718; https://doi.org/10.3390/insects14090718
Submission received: 21 June 2023 / Revised: 11 August 2023 / Accepted: 19 August 2023 / Published: 22 August 2023
(This article belongs to the Section Insect Pest and Vector Management)
Browse Figures
Review Reports Versions Notes

Abstract

:

Simple Summary

Mosquitoes carry pathogens that can cause diseases like malaria, dengue fever, chikungunya, yellow fever, and Zika fever, causing more than 700,000 deaths each year around the world. Chemical insecticides kill mosquitoes effectively, minimizing the spread of illnesses. However, these chemicals have disadvantages such as high production costs and negative impacts on the environment and other organisms, including humans. Furthermore, mosquitoes are becoming more resistant to chemical insecticides. Therefore, alternatives to commonly used insecticides are urgently required. In this review, we highlight the biotechnological potential of microorganisms to control vector mosquitoes and reduce disease transmission. In addition, we emphasize the importance of more basic research and improved translational research methods to bridge the gap between academic research on bioinsecticides and public health interventions.

Abstract

Mosquitoes transmit pathogens that cause human diseases such as malaria, dengue fever, chikungunya, yellow fever, Zika fever, and filariasis. Biotechnological approaches using microorganisms have a significant potential to control mosquito populations and reduce their vector competence, making them alternatives to synthetic insecticides. Ongoing research has identified many microorganisms that can be used effectively to control mosquito populations and disease transmission. However, the successful implementation of these newly proposed approaches requires a thorough understanding of the multipronged microorganism–mosquito–pathogen–environment interactions. Although much has been achieved in discovering new entomopathogenic microorganisms, antipathogen compounds, and their mechanisms of action, only a few have been turned into viable products for mosquito control. There is a discrepancy between the number of microorganisms with the potential for the development of new insecticides and/or antipathogen products and the actual available products, highlighting the need for investments in the intersection of basic research and biotechnology.

1. Introduction

Microorganisms constitute a large group of genetically diverse biological entities found in a wide range of terrestrial and aquatic habitats, playing crucial roles in the balance of ecosystems [1,2,3]. Advances in microbiology, molecular biology, and genomics enabled the biotechnological exploration of microbes, allowing the discovery and production of antibiotics [4,5], foods [6,7], alcoholic beverages [8], bioremediators [9,10], fertilizers [11], and biopesticides [12,13]. The microorganisms associated with mosquitoes have drawn special attention to their potential applications in public health (Figure 1) [14,15,16]. In this review, we highlight the largely unexplored potential of microbes for the control of mosquito-borne diseases and the need for improved translational research strategies, encouraging efforts toward bridging the gap between academic research and public health interventions.

2. Bacteria for Biological Control of Medically Important Mosquitoes

Today, chemical insecticides are used as the main tool for mosquito control [17,18] but are no longer as effective as in the past due to the selection of insecticide-resistant individuals in mosquito populations worldwide [19,20,21,22]. Furthermore, chemical insecticides harm the environment, contaminating groundwater systems through infiltration into the soil, reaching riverbeds, accumulating in fish and other animals [23], and through spraying, contaminating the air, affecting human health [24,25]. These facts emphasize the prominent need to develop new, efficient, and environmentally safe tools for the control of vector mosquitoes and the diseases they transmit.
Bacteria of the Bacillaceae family infect insects and produce toxins with insecticidal properties. Bacillus thuringiensis israelensis (Bti) and Lysinibacillus sphaericus (Lbs), the latter formerly known as Bacillus sphaericus, are widely known for their larvicidal activity against several species of mosquitoes [26,27,28,29,30]. Due to their high efficacy, safety, and the well-characterized mechanisms of action of their toxins, several strains of Bti and Lbs are included in commercially available biological larvicide formulations endorsed by organizations such as the World Health Organization [31] and the Environmental Protection Agency (EPA) in the United States of America (www.epa.gov/mosquitocontrol/bti-mosquito-control) (accessed on 12 April 2023).
The toxins of Bti and Lbs and the mechanisms associated with mosquito mortality have been extensively studied [32,33]. Briefly, in Bti, the molecules responsible for the entomopathogenic action are mainly the crystal toxins Cry4Aa, Cry4Ba, Cry10Aa, and Cry11Aa, the cytolytic toxins Cyt1Aa, and Cyt2Ba, and the P19 and P20 proteins [34,35]. Cry and Cyt toxins, also known as δ-endotoxins, when present in the midgut of mosquito larvae, are proteolytically activated by digestive proteases, bind to specific receptors on the host cell membranes, and cause cell rupture resulting in the death of infected larvae [36]. The Lbs Bin toxins [37,38,39], Mtx [40], Cry48Aa, and Cry49Aa [41] display entomopathogenic mechanisms similar to those described above for the Bti toxins [42]. Acting synergistically, these toxins result in effective and potent toxic activity against mosquitoes [43,44,45].
The metabolites of the Saccharopolyspora spinosa bacterium are also useful in the control of mosquitoes. Spinosad is a mixture of two S. spinosa metabolites, spinosyn A and spnosyn D, endorsed by the US EPA in 1997 [46,47,48]. This product operates uniquely by affecting post-synaptic nicotinic receptors related to acetylcholine and gamma-aminobutyric acid. This stimulation leads to involuntary muscle contractions, prostration with tremors, and paralysis in insects [49]. With minimal environmental and human health risks, Spinosad is widely used in integrated pest management, countering worldwide insecticide resistance [48].
Finding new microbes with larvicidal activities similar to those of Bt, Lbs and S. spinosa has been the goal of several research groups around the world. However, this endeavor has been limited by the fact that culture media do not always meet the requirements for the growth of many species of bacteria [50]. Therefore, the search for entomopathogenic bacteria is often limited to those that grow in commercially available culture media. Despite these limitations, bacterial strains that are suitable for cultivation and have larvicidal activity have been identified (Table 1).
Unfortunately, most of them have not been further investigated, developed for applicable products, or tested under field or semi-field conditions. Additional research to understand their mechanisms of action, effects on non-target organisms, and potential for large-scale production is needed. Toward these goals, live bacteria, deactivated bacteria, and fractionated cells or culture media have been tested for their larvicidal activities. For example, Bacillus safensis, Bacillus paranthracis, and Bacillus velezensis culture supernatants and crude lipopeptide extracts were shown to be toxic to Aedes aegypti (Linnaeus, 1762) [51]. Whole genome sequencing and mass spectrometry analysis of those isolated bacteria strains revealed that these microorganisms synthesize bacteriocin, beta-lactone, and terpenes potentially toxic to mosquito larvae [51]. Nineteen Bacillus sp. strains and two strains of Brevibacillus halotolerans isolated from Amazonian environments showed larvicidal activity against Ae. aegypti [52]. The supernatant and pellet fractions of those strains were tested separately, revealing that cellular and secreted metabolites are toxic to mosquito larvae; however, the active molecules were not identified. In another study, Bacillus sp. EG6.4 culture exhibited high toxicity to Ae. aegypti larvae. Transmission electron microscopy revealed subterminal oval-shaped endospores and massive parasporal inclusions unrelated to cry toxin. The bacterium showed hemolytic activity, indicating its potential to produce biosurfactants. Detection of the surfactin-coding gene (srfA-D) confirmed its association with B. mojavensis strain PS17. These findings suggest that biosurfactant production, particularly surfactin, may play a role in Bacillus sp. EG6.4’s larvicidal mechanism [53]. The testing of whole or fractionated bacteria and culture media is useful for defining procedures and formulation of new biolarvicides.
Table 1. Bacterial strains active against Aedes, Culex, and/or Anopheles mosquito larvae.
Table 1. Bacterial strains active against Aedes, Culex, and/or Anopheles mosquito larvae.
BacteriumToxic FormulationTarget Mosquito GeneraRefs.
AedesCulexAnopheles
Bacillus thuringiensis var. israelensis (Bti)Extract (spores and crystals)+−−[54]
Sporulated culture powder (tablet formulation XL-47)+−−[55]
Spores and crystals tablet+−−[56]
Spores and crystals tablet+−−[57]
VectoBac WG *+−−[58]
Formulated product−+−[59]
Binary mixtures (Bti plus Deltamethrin)−+−[60]
Cry2Aa and Cyt1Aa crystals −+−[61]
Crystallogenic variants.++−[62]
Two recombinant proteins (Cry10Aa and Cyt2Ba)+−−[63]
Xpp81Aa toxin combined with Cry2Aa and Cry4Aa +−−[35]
Kappa-carrageenan and Vectobac 12 AS hydrogels *+−−[64]
Bti extracts +−−[65]
Vectobac® AS * + and plant-ethanol extracts−+−[66]
Granular formulation (Vectobac G) *−−+[67]
Dispersible granule (strain AM65-52) *+++[68]
Bti strain Becker Microbial products (BMP) *−++[69]
Bti sprayed products BACTIMOS WP® *; VECTOBAC TP® *; and TEKNAR® HP-D *−−+[70]
Bti water dispersible granular (WDG) VectoBac@ strain AM65-52 *−−+[71,72,73,74]
Bacillus thuringiensis (Other strains)Total and lyophilized culture++−[75]
Bacterial cultures+++[76]
Bacterial suspensions (spores and crystals)+−−[77]
Spores+++[78,79]
Parasporal crystalline inclusion bodies+−−[35]
Culture supernatant+−+[29]
Synergistic interaction (Purified Cry11Aa and Cyt1Aa Toxins)+−−[80]
Synergistic action of the Cry and Cyt proteins−−+[81]
Lysinibacillus sphaericus (Lbs)Culture supernatant+−+[29]
Spores and vegetative cells++−[30]
Cell suspension plus glyphosate+−−[82]
Spore crystals (lyophilized powder)+++[83]
Spores-+-[84]
Granular formulation (Vectobac G) *−++[67]
Vectolex G *−+−[85]
S-layer protein−+−[86]
Purified BinA and BinB proteins−++[87,88]
Spore crystals and purified S-layers protein−++[89]
Synergy of Mtx and Cry proteins−+−[44]
Purified BinA and BinB proteins−+−[39]
VectoLex® * WG plus Pyrethroid Resigen®−+−[90]
Cry48Aa and Cry49Aa proteins combined−+−[91]
Synergistic interaction (S-Layer and spores/crystals)−+−[92]
VectoLex (ABG-6185) *−−+[93]
Suspension (lyophilized bacteria)−−+[94]
VectoLex® CG *−−+[95]
Bin toxin proteins−−+[96]
Acidovorax sp.Cell-free supernatant+−−[97]
Aneurinibacillus aneurinilyticusBacterial suspension+++[98]
Bacillus amyloliquefaciensBiosurfactant+++[99]
Bacillus cereusCulture supernatant+−+[29]
Bacillus circulansSpores+++[100]
Brevibacillus halotoleransSupernatant and pellet fractions of bacterial cultures+−−[52]
Bacillus licheniformisDahb1 exopolysaccharide (Bl-EPS)+−+[101]
Brevibacillus laterosporusSuspension of sporulated cells+−+[102]
Spore and the canoe-shaped parasporal body (CSPB) structure+−−[103]
Purified protein crystals+−+[104]
Pellets (cells and spores)+−−[105]
Spores+−−[106]
Bacillus paranthracisPellets (cells)+−−[51]
Bacillus safensisSupernatant and pellet fractions of bacterial cultures+−−[52]
Pellets (cells)+−−[51]
Bacillus subtilisCulture supernatant+−+[29]
Crude cyclic lipopeptides (CLPs)−+−[107]
Crude surfactin−−+[108]
Bacterial biomass+−−[109]
Biosurfactants−−+[110,111]
Bacillus megateriumBacterial culture+−−[52]
Bacillus nealsoniiSecondary metabolites+−−[112]
Bacillus tequilensisCyclic lipopeptide Biosurfactant−−+[113]
Bacillus velezensisBacterial culture+−−[52]
Pellets (cells)+−−[51]
Chromobacterium sp.Hydrogen cyanide+−+[114,115]
Chromobacterium anophelisBacterial suspension−−+[116]
Pantoea stewartiiSilver nanoparticles+++[117]
Paraclostridium bifermentansClostridial neurotoxin−−+[118]
Peanibacillus maceransBacterial biomass+−−[109]
Photorhabdus luminescensSecondary metabolites (Culture fluids)+−−[119]
Secondary metabolites+−−[120]
Photorhabdus luminescens subsp. akhurstiiBacterial cell suspension+−−[121]
Pseudomonas sp.Bacterial cell suspension−+−[88]
Priestia aryabhattaiSilver nanoparticles+++[117]
Serratia marcescensProdigiosin+−+[122,123]
Bacterial suspension+−−[124]
Serratia nematodiphilaBacterial cultures+++[76]
Saccharopolyspora spinosaSpinosad (Tracer®) *+−+[125]
Spinosad formulation+++[46]
Spinosad-based product (Laser®) *+++[126]
Spinosad SC (Tracer®) *+−−[127]
Spinosad tablet (DT) and granules (GR) *+−−[128]
Spinosad powder *−+−[129]
Spinosad formulation *−−+[130,131]
Natular T-30 formulation *−+−[132]
Formulation emulsifiable Concentrate−+−[133]
Streptomyces sp.Secondary metabolites+−−[112,134]
Xenorhabdus indicaBacterial cell suspension+−−[121]
Xenorhabdus nematophilaSecondary metabolites+−−[120]
Secondary metabolites (culture fluids)+−−[119]
Xenorhabdus stockiaeBacterial cell suspension+−−[121]
This list is not exhaustive but provides ideas for future research and product development opportunities. The asterisks (*) indicate products already registered and authorized for commercial use.”+” sign indicates the toxic action of bacteria or their metabolic products on the target mosquito. “−” sign indicates absence of action due to the study not targeting the mosquito in question.

3. Fungi and Promising Approaches for Controlling Vector Mosquitoes and Plasmodium spp.

Fungi and their metabolites are potentially useful for the control of medically important mosquitoes [135,136,137,138,139,140]. In fact, fungal strains have already been applied as complementary measures for the control of vector mosquitoes [141,142,143,144]. The identification of mosquito fungi with larvicidal activities (Table 2), highlights the potential for their application as tools in mosquito management.
Beauveria bassiana strains infect and kill a variety of insects, including mosquitoes. Application of B. bassiana spores on surfaces where mosquitoes rest [145], the impregnation of spores in traps [146], the association of the fungus with insecticides, such as the combination of B. bassiana and permethrin [147], and the spread of the fungus by females mating with pre-inoculated males [148] have been proposed as means of field applications of B. bassiana against mosquitoes. The attraction of An. stephensi to spores of B. bassiana present in dead and dying caterpillars infected with the fungus [149] has been proposed as a useful alternative to infect mosquitoes. Furthermore, experimental evolution has been applied successfully to increase the efficacy of B. bassiana to Anopheles coluzzii (Coetzee et al., 2013) [150].
Exposure to lethal and sublethal doses of B. bassiana spores decreases adult Ae. aegypti and Aedes albopictus (Skuse, 1894) host-seeking behavior and fecundity [135,151]. Infected mosquitoes, while still alive, spread the fungus through the vector population. Beauveria bassiana spores and extracts are also effective against mosquito larvae [152,153,154]. As a result of this evidence, several strains of B. bassiana are authorized for use as biological insecticides, against vector mosquitoes, by regulatory agencies such as the EPA [155] and ANVISA in Brazil [156].
Metarhizium anisopliae is another fungus with biotechnological potential for mosquito control [157]. Its entomopathogenic mechanism is similar to that of B. bassiana. After contact, the spores germinate, producing hyphae, which penetrate the insect exoskeleton and develop inside the host’s body [158,159].
Metarhizium anisopliae CN6S1W1 is effective against Ae. albopictus and Cx. pipiens [160]. The fungus also affects the behavior of An. gambiae mosquitoes by inhibiting blood feeding and reducing fecundity and oviposition [161]. Concurrent infections with both M. anisopliae and B. bassiana shorten the lifespan of Ae. aegypti [145,162]. The synergistic actions of M. anisopliae and B. bassiana, together with the imidacloprid immunosuppressant, showed greater larvicidal activity against Cx. quinquefasciatus than the respective entomopathogens alone [163]. Suspensions of M. anisopliae-VKKH3 conidia were highly toxic to Ae. aegypti, An. stephensi, and Cx. quinquefasciatus larvae. It was observed that the larvae were completely invaded by conidia, which formed mycelium and were able to multiply and intensely invade the larval tissues, with the highest virulence observed at a dose of 1010 conidia/mL [138]. Ethyl acetate extracts from M. anisopliae are active against mosquito larvae. The metabolites contained in those extracts have not been identified but they may represent a solution for mosquito larvae control, since M. anisopliae conidia are not effective in the aquatic environment [164].
In addition to B. bassiana and M. anisopliae, other fungi have been reported with high biotechnological potential for mosquito control. The killing activity of Aspergillus nomius spores toward adult Ae. albopictus was comparable to those of B. bassiana [165]. Crude and purified extracellular extracts of Aspergillus niger with larvicidal action against An. stephensi, Cx. quinquefasciatus, and Ae. aegypti were reported [166]. Di-N-Octyl phthalate, (1H-Benzoimidazole-2-Yl)-[4-(4-Methyl-Piperazin-1-Yl)-Phenyl]-Amine, and 6,8-Dimethyl-5-Oxo-2,3,5,8-Tetrahydroimidazo [1,2-A] Pyrimidine, secondary metabolites of Aspergillus flavus and Aspergillus fumigatus [167] and preg-4-en-3-one, 17. α-hydroxy-17. β-cyano-, trans-3-undecene-1,5-diyne, and pentane, 1,1,1,5-tetrachloro-, from Aspergillus tamarii have been suggested to be responsible for larvicidal activity [168]. The biosafety of products derived from Aspergillus spp., or the fungus itself, still needs to be investigated. Suspensions of A. flavus conidia exhibited considerable toxicity against non-target organisms present in aquatic environments of mosquito larvae [169].
Species of the genus Isaria also have entomopathogenic characteristics for mosquito control. Isaria tenuipes [170], Isaria javanica ARSEF 5874, and Isaria cateniannulata ARSEF 6241 strains showed high levels of pathogenicity toward Ae. aegypti [137]. Larvicidal activity against Cx. quinquefasciatus and Ae. aegypti were demonstrated with silver nanoparticles (AgNps) carrying secondary metabolites of Isaria fumosorosea (Ifr) [171]. Other fungal species of interest that may be useful for vector control include Trichoderma asperellum [172] and Hyalodendriella sp. [173] which produce metabolites toxic to mosquitoes.
Table 2. Fungal strains active against Aedes, Culex, and/or Anopheles mosquito larvae.
Table 2. Fungal strains active against Aedes, Culex, and/or Anopheles mosquito larvae.
FungusToxic FormulationTarget Mosquito GeneraRefs.
AedesCulexAnopheles
Beauveria bassianaMycotrol ESO *+−−[174]
Fungal suspensions+−−[145]
Surfaces treated with conidia+−−[148]
Spores+−−[135]
Oil-formulated spores−−+[149]
Fungal suspensions−−+[152]
Spores−−+[150]
Fungal suspensions++−[175]
Metarhizium anisopliaeConidial suspension−+−[176]
Fungal conidia+−−[177]
Fungal suspensions+−−[145]
Conidial suspension++−[160]
Oil formulation−++[178]
Secondary metabolites+++[179]
Aspergillus nigerCrude metabolites+++[166]
Aspergillus flavusSecondary metabolites+++[167]
Suspensions of conidia+-−[169]
Culture filtrates−+−[180]
Aspergillus fumigatusSecondary metabolites+++[167]
Aspergillus parasiticusCulture filtrates−+−[180]
Aspergillus tamariiEndophytic fungal extracts++−[168]
Aspergillus terreusMycelia (ethyl acetate and methanol extracts)+++[181]
Emodin compound+++[182]
Aspergillus nomiusSpores+−−[165]
Beauveria tenellaBlastospores suspensions++−[183]
Cladophialophora bantianaSecondary metabolites++−[184]
Chrysosporium lobatumSecondary metabolites−++[185]
Chrysosporium tropicumSecondary metabolites+++[186]
Fusarium moniliformeIsoquinoline type pigment+−+[187]
Fusarium oxysporumTemephos + F. oxysporum extract+++[188]
Fusarium vasinfectumCulture filtrates−+−[180]
Isaria javanicaConidial suspensions+−−[137]
Isaria cateniannulataConidial suspensions+−−[137]
Isaria tenuipesConidial suspensions+−−[170]
Isaria fumosoroseaSecondary metabolites++−[171]
Paecilomyces sp.Secondary metabolites+++[134]
Penicillium daleaeMycelium extract++−[189]
Penicillium falicumCulture filtrates−+−[180]
Penicillium marneffeiSpores−+−[190]
Penicillium sp.Ethyl acetate extract−+−[191]
Ethyl acetate extract++−[192]
Pestalotiopsis virgulataEthyl acetate mycelia (EAM) extracts and liquid culture media (LCM)+−+[193]
Podospora sp.Sterigmatocystin compound−−+[194]
Pycnoporus sanguineusEthyl acetate mycelia (EAM) extracts and liquid culture media (LCM)+−+[193]
Trichoderma asperellumMethanolic extract−−+[172]
Trichoderma harzianumMycosynthesized silver nanoparticles (Ag NPs)+−−[195]
Trichoderma virideCulture filtrates−+−[180]
Hyalodendriella sp.EtOAc extract+−−[173]
Verticilluim lecaniiSpores−+−[190]
Conidia−−+[196]
This list is not exhaustive but provides ideas for future research and product development opportunities. The asterisks (*) indicate products already registered and authorized for commercial use.”+” sign indicates the toxic action of bacteria or their metabolic products on the target mosquito. “−” sign indicates absence of action due to the study not targeting the mosquito in question.

The Potential of Fungi as Anti-Plasmodium Agents for Malaria Control

Fungi with potential antiparasitic properties, particularly against protozoa of the genus Plasmodium, have been researched as a potential tool to combat malaria. Endophytic fungi isolated from different organs of Annona muricata, a medicinal plant commonly used in traditional Cameroonian medicine against malaria, completely inhibited the growth of P. falciparum in vitro. Of the 152 fungi tested, 17.7% showed activities against different strains of the parasite, with the strongest effects from fungi belonging to the genus Fusarium, Thricoderma, Aspergillus, Penicillium, and Neocosmopora [197]. Compounds such as oxylipin and alternarlactones from Penicillium herquei and Alternaria alternata, respectively, demonstrated in vitro antiplasmodial activity [198,199]. A killer toxin purified from Wickerhamomyces anomalus, a symbiotic yeast of insects, when supplemented in a mosquito diet interfered with the development of ookines in the An. Stephensi midgut [200]. Aspergillus also showed antiplasmodial activity when supplemented in the mosquito diet. This activity was shown to be related to the inhibition of the interaction between parasites and fibrinogen-related protein-1 (FREP1), an agonist of gametocytes and ookinetes [201]. These authors identified the fungal metabolite, orlandin, as a candidate reagent to inhibit P. falciparum infection in An. gambiae.
The topical application or spraying of B. bassiana on the mosquito cage mesh killed ~92% of An. stephensi on day 14 after exposure and reduced the number of Plasmodium chabaudi sporozoite-positive mosquitoes. Although no impact on the early stages of the parasite (gametocytes and oocyst stages) was noted, the combined effect of mosquito mortality and reduced sporozoite prevalence was estimated to result in the reduction in malaria transmission risk by a factor of about 80 [202]. However, other studies did not reproduce these results and the differences in the outcomes could be related to the differences in experimental conditions and in both mosquito and parasite strains. Further consideration of these fungi in antimalarial campaigns would require further in-depth research to identify potential factors contributing to the observed differences in the impacts of B. bassiana and M. anisopliae on the development of Plasmodium species in Anopheles mosquitoes [203,204].

4. The Role of Insect-Microbiota Associations in Vector Competence

Associations between mosquitoes and their microbiota have gained significant attention in scientific research due to their impact on vector competence [205,206,207,208,209,210]. In the following, we discuss ways these associations can influence vector competence. Understanding these interactions is essential for developing effective vector-borne disease control strategies and reducing their impact on public health.

4.1. Symbiotic Bacteria and Their Potential against Infectious Agents

The mosquito microbiota influences host development, nutrition, reproduction, and immune responses to invading organisms [211,212,213,214]. While the composition of the mosquito microbiota is largely defined by the environment in which they live [215,216,217], resident bacteria can modulate the development and replication of parasites and viruses within their vectors [218,219,220,221,222,223,224,225]. Although this modulation can enhance or reduce the survival and replication of pathogens within mosquitoes, those mosquito–microbiota interactions that negatively affect pathogens offer possibilities to control arthropod-borne diseases.
For example, the Gram-negative bacteria, Escherichia coli H243, E. coli HB101, Pseudomonas aeruginosa, and Ewingella americana inhibit the formation of Plasmodium falciparum oocysts, in Anopheles stephensi (Liston, 1901) [226]. Enterobacter sp. (Esp_Z) isolated from the intestine of Anopheles gambiae (Giles, 1902) inhibited the development of malaria parasites when reintroduced into this same vector species [227,228]. The formation of oocysts of Plasmodium berghei was affected by the presence of Serratia marcescens-HB3 in An. stephensi [229]. In An. gambiae, Escherichia coli, S. marcescens, and Pseudomonas stutzeri reduced the prevalence and intensity of P. falciparum infection [230]. The Serratia Y1 strain exerts inhibitory activity on P. berghei ookinetes by activation of the Toll immune pathway in An. stephensi [231]. Serratia ureilytica (Su_YN1) produces an antimalarial lipase (AmLip) that inhibits the formation of P. falciparum oocysts in An. stephensi and An. gambiae [232]. Asaia SF2.1 also inhibits Plasmodium development in anophelines [233].
Virus replication in their vectors is also regulated by the mosquito microbiota. Bacteria of the genera Proteus, Paenibacillus, and Chromobacterium inhibited the replication of dengue virus serotype 2 (DENV-2) when administered to mosquitoes [114,234]. Some of the mechanisms by which symbiotic bacteria can hamper pathogen development have been elucidated and can be exploited to inhibit the spread of infectious agents by mosquitoes (Figure 2).

4.2. Wolbachia-Based Strategy for Controlling Mosquito-Borne Viruses: Mechanisms, Efficacy, and Implications

The wMel and wAlbB strains of Wolbachia pipientis, an intracellular bacterium, inhibit dengue, CHIKUNGUNYA, and Zika virus replication within mosquito cells [235,236,237,238,239]. However, another Wolbachia strain, wPip, does not inhibit virus infection in Ae. aegypti [240] and the mechanism by which Wolbachia interferes with virus replication has not been fully elucidated. Current hypotheses include competition between Wolbachia and the virus for physical space within mosquito cells and metabolite resources [241,242] and Wolbachia-induced modulation of the host’s immune system and immune priming. Immune priming entails sensitizing or preparing the mosquito’s immune system for a faster and more efficient response to a specific pathogen, such as a virus, upon subsequent exposure [243,244].
Despite the lack of a complete understanding of the mechanism or mechanisms involved in Wolbachia-associated modulation of viral suppression, the Wolbachia-carrying mosquito-based strategy has been deployed as a public health intervention to control dengue transmission (The World Mosquito Program https://www.worldmosquitoprogram.org/) (accessed on 15 February 2023). A randomized study carried out in the city of Yogyakarta, Indonesia, compared the areas where Ae. aegypti carrying Wolbachia was released with areas without Wolbachia. The results revealed a 77% lower incidence of dengue cases, in the Wolbachia-treated area [245]. Another study conducted in the city of Niterói, Rio de Janeiro, Brazil, reported a 69% reduction in dengue, 56% in chikungunya, and a 37% reduction in Zika incidence three years after the beginning of the release of Ae. aegypti with Wolbachia [246].
Although these results bring optimism regarding the use of Wolbachia for the control of dengue transmission, these bacteria can have variable effects on mosquito-borne viruses. For example, the Wolbachia strain wMel strongly blocked Mayaro virus (MAYV) infections in Ae. aegypti, but another strain, wAlbB, did not influence MAYV infection in this same vector. Aedes aegypti infected with wAlbB and wMel showed enhanced Sindbis virus infection rates [247]. The variable effects of Wolbachia on vector competence bring into question the safety of the current release of Wolbachia-infected mosquitoes. Furthermore, the potential impact of these bacteria on biodiversity has not been thoroughly investigated [248,249], and the risk of the emergence of DENV variants that escape virus-specific inhibition in Wolbachia-infected mosquitoes [250,251], underscores the importance of further research on interactions between Wolbachia, mosquitoes, viruses, and other organisms.

4.3. Symbiotic Microorganisms and Paratransgenesis

Paratransgenesis involves the colonization of vector insects with genetically engineered symbiotic microorganisms that are effective in inhibiting parasite development [252,253,254,255]. Ideal symbionts for effective paratransgenesis are easily manipulated genetically, colonize mosquitoes efficiently, spread into mosquito populations (vertical and horizontal transmission), and are efficient in inhibiting pathogen development in mosquitoes [256]. Proof-of-principle experiments performed primarily with bacteria demonstrated that genetically modified microorganisms expressing antipathogen molecules are capable of interfering with or blocking the development of malaria parasites in mosquitoes [257,258,259]. Among the mosquito symbiotic bacteria, strains of Asaia, Pantoea, Serratia, Pseudomonas, and Thorsellia have been evaluated as candidates for paratransgenesis [260,261,262,263,264].
The fungus Metarhizium anisopliae has been genetically transformed to express anti-Plasmodium proteins. Mosquitoes treated with transgenic M. anisopliae had 71–98% fewer sporozoites present in their salivary glands [204]. Scorpine, one of the molecules expressed by transgenic M. anisopliae, also affects negatively dengue virus replication, expanding the application of genetically transformed fungi to control arbovirus transmission [265].
Densovirus, a small DNA virus (4–6 kb) belonging to the Parvoviridae family (Densovirinae subfamily), infects arthropods such as mosquitoes and is maintained in natural populations through both horizontal and vertical transmission from infected adults to larvae. With one of the smallest known viral genomes, Densovirus serves as a valuable molecular tool. Its compact genome can be inserted into an infectious plasmid, which can then be used to express antiparasitic genes, both in cell cultures and in live mosquitoes [266,267,268,269].
The discovery of mosquito symbiotic bacteria [258,270,271,272], viruses [266,267,268,269], and fungi [273] is an active area of research. Advances toward deploying paratransgenesis as a tool for blocking pathogen transmission by mosquitoes also include the identification of antipathogen effector peptides and mechanisms of cellular secretion [253,258]. In bacteria, one efficient way of secreting effector molecules from the bacterial cytoplasm into the lumen of the mosquito intestine was engineered using Escherichia coli’s hemolysin-A secretion system. This process involves the export of proteins, such as hemolysin HlyA, through a specific mechanism that includes an export signal at the C-terminal end of the protein, along with the membrane proteins HlyB, HlyD, and the outer membrane protein TolC [274]. The use of bacteria for paratransgenesis is the most advanced alternative compared with viruses and fungi applications. However, concerns about the safety of releasing engineered bacteria into the environment and the potential unforeseen consequences still require attention when contemplating field tests for paratransgenesis.
Self-limiting paratransgenesis [256] has been suggested as an alternative for initial field trials. This approach proposes the utilization of transient expression of antipathogen compounds from a plasmid that is gradually lost, reverting bacteria to their original wild type. Risk assessment still needs to be carried out and laws and regulations need to be created and enacted before paratransgenesis can be tested in field conditions. However, the processes by which genetically modified microorganisms (GMs) can be spread in nature and how they should act to inhibit the development of target parasites in mosquitoes have already been envisaged. This is illustrated in Figure 3, which presents the paratransgenesis process as a multifaceted approach to combating mosquito-borne diseases.

5. Roadmap for the Development of Microbe-Based Products for Controlling Mosquito-Borne Diseases

In this review article, we explored the biotechnological potential of microorganisms for mosquito population control and reduction in vector competence. We listed many microbial agents with mosquito larvicidal activity and provide information on their active metabolites and mechanisms of action. However, most of these mosquitocidal microorganisms and their metabolites have not been developed into new products and marketed as tools and innovations that can be applied to public health interventions. The explanation for the few biolarvicides available on the market is complex and is determined by technical, regulatory, social, and economic factors.
For example, the Organization for Economic Co-operation and Development (OECD) provides information about requirements and approaches to biological pesticides (https://www.oecd.org/env/ehs/pesticides-biocides/data-for-biopesticide-registration.htm) (accessed on 14 July 2023) including a Guidance for Registration Requirements for Microbial Pesticides (https://one.oecd.org/document/env/jm/mono(2003)5/en/pdf) (Aaccessed on 14 July 2023). Accordingly, the Regulation of European Commission (EC) No. 1107/2009 regarding criteria for the approval of microbial pesticides emphasizes the importance of assessing the active substances or the microorganisms themselves for effects on the environment or harmful effects on human or animal health [275]. These directives require collaborative research efforts which may take years to complete. In the United States, the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) requires similar assessments, and the U.S. Environmental Protection Agency (EPA) evaluates biopesticides to assure they do not pose unreasonable risks of harm to human health and the environment.
In Brazil [276], the registration of new biopesticides, including biolarvicides, requires evaluation by three federal government agencies that assess them independently and in a specific manner. The Ministry of Agriculture and Livestock (Ministério da Agricultura e Pecuária-MAP, Brasília, DF, Brazil) evaluates efficiency and potential for use in pest control; the Brazilian Institute of the Environment and Renewable Natural Resources (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis-IBAMA, Brasília, DF, Brazil) provides an environmental report; and the Brazilian Health Regulatory Agency (Agência Nacional de Vigilância Sanitária-ANVISA, Brasília, DF, Brazil) conducts the toxicological dossier, assessing the product’s toxicity for the population and the restrictions and requirements for biopesticide use.
The main stages for discovering and developing new larvicides, based on the requirements set forth by government entities, have previously been reviewed [277,278,279]. In summary, the process consists of (1) discovering larvicidal microorganisms; (2) identifying the mechanisms of action of larvicidal microorganisms (live microbial fractions versus metabolites fractions); (3) evaluating human toxicity and pathogenicity of microorganisms and evaluating their effects on non-target organisms and the environment; (4) determining the stability of the candidate larvicide product under field conditions and its shelf life considering its applications in tropical/subtropical, hot and humid environments; (5) comparing the activity of the candidate product with currently available larvicides; and (6) cost analysis (production, storage, transportation, and field application costs) and research of market viability.
Similar considerations will be necessary for the applications designed for reducing disease transmission, such as the deployment of microorganisms with larvicidal and/or antipathogen activity, including paratransgenesis discussed above.
We hope that this review will encourage additional research and investment in the development of new bioinsecticides, highlighting the need to follow the requirements established by regulatory agencies for the approval and registration of products that will assist in the control of mosquitoes and the diseases they transmit.

6. Final Considerations

Biotechnological approaches using microorganisms have significant potential to control mosquito populations and reduce their vector competence, making them alternatives to synthetic insecticides. The ongoing research has been crucial in identifying new products and approaches that can be used effectively to control disease transmission. However, the successful implementation of these newly proposed approaches requires a thorough understanding of the multipronged microorganism–mosquito–pathogen–environment interactions. The release of mosquitoes or microorganisms, genetically modified or not, into the environment requires an assessment of the associated risks and benefits. Therefore, the environmental and ethical implications of these proposed releases are active areas of debate [280,281].
Although much has been achieved in discovering new entomopathogenic microorganisms, antipathogen compounds, and their mechanisms of action, reviewed above, only a few have been turned into viable products for mosquito control. There is a discrepancy between the number of microorganisms with potential for the development of new products and the actual available products, highlighting the need for investments in the intersection of research and biotechnology to improve the transition of basic into applied research.

Author Contributions

Writing—review and editing, R.d.M.K., E.M.R., O.M., B.C.B., A.M.C. and J.A.S.-N.; supervision, E.M.R. and O.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Human Frontier Science Program Research Grant RGP0007/2017 to J.A.S.N.; by the São Paulo Research Foundation (FAPESP), 2020/06136-5 to J.A.S.N., and to Prodoc-AM/FAPEAM-003/2022 for providing the scholarship that benefited author R.MK.

Data Availability Statement

The data presented in this study are openly available in this manuscript.

Conflicts of Interest

The authors declare that they have no conflict of interest.

References

  1. Onen, O.; Aboh, A.A.; Mfam, A.N.; Akor, M.O.; Nweke, C.N.; Osuagwu, A.N. Microbial Diversity: Values and Roles in Ecosystems. Asian J. Biol. 2020, 9, 10–22. [Google Scholar]
  2. Rousk, J.; Bengtson, P. Microbial Regulation of Global Biogeochemical Cycles. Front. Microbiol. 2014, 5, 103. [Google Scholar] [CrossRef] [PubMed]
  3. Rodríguez-Frías, F.; Quer, J.; Tabernero, D.; Cortese, M.F.; Garcia-Garcia, S.; Rando-Segura, A.; Pumarola, T. Microorganisms as Shapers of Human Civilization, from Pandemics to Even Our Genomes: Villains or Friends? A Historical Approach. Microorganisms 2021, 9, 2518. [Google Scholar] [CrossRef] [PubMed]
  4. Raaijmakers, J.M.; Vlami, M.; De Souza, J.T. Antibiotic Production by Bacterial Biocontrol Agents. Antonie Leeuwenhoek 2002, 81, 537–547. [Google Scholar] [CrossRef] [PubMed]
  5. Uchida, R.; Imasato, R.; Tomoda, H.; Ōmura, S. Yaequinolones, New Insecticidal Antibiotics Produced by Penicillium sp. FKI-2140. J. Antibiot. 2006, 59, 652–658. [Google Scholar] [CrossRef]
  6. Bintsis, T. Lactic Acid Bacteria: Their Applications in Foods. J. Bacteriol. Mycol. 2018, 6, 89–94. [Google Scholar]
  7. Barzee, T.J.; Cao, L.; Pan, Z.; Zhang, R. Fungi for Future Foods. J. Future Foods 2021, 1, 25–37. [Google Scholar] [CrossRef]
  8. Torres-Guardado, R.; Esteve-Zarzoso, B.; Reguant, C.; Bordons, A. Microbial Interactions in Alcoholic Beverages. Int. Microbiol. 2022, 25, 1–15. [Google Scholar] [CrossRef]
  9. Sevak, P.I.; Pushkar, B.K.; Kapadne, P.N. Lead Pollution and Bacterial Bioremediation: A Review. Environ. Chem. Lett. 2021, 19, 4463–4488. [Google Scholar] [CrossRef]
  10. Cowan, A.R.; Costanzo, C.M.; Benham, R.; Loveridge, E.J.; Moody, S.C. Fungal Bioremediation of Polyethylene: Challenges and Perspectives. J. Appl. Microbiol. 2022, 132, 78–89. [Google Scholar] [CrossRef]
  11. Jiménez-Gómez, A.; García-Estévez, I.; Escribano-Bailón, M.T.; García-Fraile, P.; Rivas, R. Bacterial Fertilizers Based on Rhizobium laguerreae and Bacillus halotolerans Enhance Cichorium endivia L. Phenolic Compound and Mineral Contents and Plant Development. Foods 2021, 10, 424. [Google Scholar] [CrossRef] [PubMed]
  12. Dunham, B. Microbial Pesticides: A Key Role in the Multinational Portfolio. New Ag Int. 2015, 32–36. [Google Scholar]
  13. Ruiu, L. Microbial Biopesticides in Agroecosystems. Agronomy 2018, 8, 235. [Google Scholar] [CrossRef]
  14. Thongsripong, P.; Chandler, J.A.; Green, A.B.; Kittayapong, P.; Wilcox, B.A.; Kapan, D.D.; Bennett, S.N. Mosquito Vector-associated Microbiota: Metabarcoding Bacteria and Eukaryotic Symbionts across Habitat Types in Thailand Endemic for Dengue and Other Arthropod-borne Diseases. Ecol. Evol. 2018, 8, 1352–1368. [Google Scholar] [CrossRef] [PubMed]
  15. da Silva Gonçalves, D.; Iturbe-Ormaetxe, I.; Martins-da-Silva, A.; Telleria, E.L.; Rocha, M.N.; Traub-Csekö, Y.M.; O’Neill, S.L.; Sant’Anna, M.R.V.; Moreira, L.A. Wolbachia Introduction into Lutzomyia longipalpis (Diptera: Psychodidae) Cell Lines and Its Effects on Immune-Related Gene Expression and Interaction with Leishmania infantum. Parasites Vectors 2019, 12, 33. [Google Scholar] [CrossRef]
  16. Caragata, E.P.; Short, S.M. Vector Microbiota and Immunity: Modulating Arthropod Susceptibility to Vertebrate Pathogens. Curr. Opin. Insect Sci. 2022, 50, 100875. [Google Scholar] [CrossRef]
  17. Chavasse, D.C.; Yap, H.H.; World Health Organization. Chemical Methods for the Control of Vectors and Pests of Public Health Importance; World Health Organization: Geneva, Switzerland, 1997.
  18. Wilson, A.L.; Courtenay, O.; Kelly-Hope, L.A.; Scott, T.W.; Takken, W.; Torr, S.J.; Lindsay, S.W. The Importance of Vector Control for the Control and Elimination of Vector-Borne Diseases. PLoS Neglected Trop. Dis. 2020, 14, e0007831. [Google Scholar] [CrossRef]
  19. Rawlins, S.C.; Wan, J.O. Resistance in Some Caribbean Populations of Aedes aegypti to Several Insecticides. J. Am. Mosq. Control Assoc. 1995, 11, 59–65. [Google Scholar]
  20. Nauen, R. Insecticide Resistance in Disease Vectors of Public Health Importance. Pest Manag. Sci. Former. Pestic. Sci. 2007, 63, 628–633. [Google Scholar] [CrossRef]
  21. Hamid, P.H.; Prastowo, J.; Ghiffari, A.; Taubert, A.; Hermosilla, C. Aedes aegypti Resistance Development to Commonly Used Insecticides in Jakarta, Indonesia. PLoS ONE 2017, 12, e0189680. [Google Scholar] [CrossRef]
  22. Lopes, R.P.; Lima, J.B.P.; Martins, A.J. Insecticide Resistance in Culex quinquefasciatus Say, 1823 in Brazil: A Review. Parasites Vectors 2019, 12, 591. [Google Scholar] [CrossRef] [PubMed]
  23. Kaushal, J.; Khatri, M.; Arya, S.K. A Treatise on Organophosphate Pesticide Pollution: Current Strategies and Advancements in Their Environmental Degradation and Elimination. Ecotoxicol. Environ. Saf. 2021, 207, 111483. [Google Scholar] [CrossRef] [PubMed]
  24. Costa, L.G. Current Issues in Organophosphate Toxicology. Clin. Chim. Acta 2006, 366, 1–13. [Google Scholar] [CrossRef] [PubMed]
  25. Naughton, S.X.; Terry, A.V., Jr. Neurotoxicity in Acute and Repeated Organophosphate Exposure. Toxicology 2018, 408, 101–112. [Google Scholar] [CrossRef] [PubMed]
  26. Margalith, Y.; Ben-Dov, E. Biological control by Bacillus thuringiensis subsp. israelensis. In Insect Pest Management: Techniques for Environmental Protection; Rechcigl, J.E., Rechcigl, N.A., Eds.; CRC Press: Boca Raton, FL, USA, 2000; pp. 243–301. [Google Scholar]
  27. Polanczyk, R.A.; de Garcia, M.O.; Alves, S.B. Potencial de Bacillus thuringiensis israelensis Berliner No Controle de Aedes aegypti. Rev. Saúde Pública 2003, 37, 813–816. [Google Scholar] [CrossRef] [PubMed]
  28. Boyce, R.; Lenhart, A.; Kroeger, A.; Velayudhan, R.; Roberts, B.; Horstick, O. Bacillus thuringiensis israelensis (Bti) for the Control of Dengue Vectors: Systematic Literature Review. Trop. Med. Int. Health 2013, 18, 564–577. [Google Scholar] [CrossRef]
  29. Balakrishnan, S.; Indira, K.; Srinivasan, M. RETRACTED ARTICLE: Mosquitocidal Properties of Bacillus Species Isolated from Mangroves of Vellar Estuary, Southeast Coast of India. J. Parasit. Dis. 2015, 39, 385–392. [Google Scholar] [CrossRef]
  30. Santana-Martinez, J.C.; Silva, J.J.; Dussan, J. Efficacy of Lysinibacillus sphaericus against Mixed-Cultures of Field-Collected and Laboratory Larvae of Aedes aegypti and Culex quinquefasciatus. Bull. Entomol. Res. 2019, 109, 111–118. [Google Scholar] [CrossRef]
  31. World Health Organization. Report of the Seventh WHOPES Working Group Meeting; 2–4 December 2003: Review of: Vectobac WG Permanet Gokilaht-S 5EC; WHO/HQ: Geneva, Switzerland, 2004.
  32. Bravo, A.; Gill, S.S.; Soberón, M. Mode of Action of Bacillus thuringiensis Cry and Cyt Toxins and Their Potential for Insect Control. Toxicon 2007, 49, 423–435. [Google Scholar] [CrossRef]
  33. Adang, M.J.; Crickmore, N.; Jurat-Fuentes, J.L. Diversity of Bacillus thuringiensis Crystal Toxins and Mechanism of Action. In Advances in Insect Physiology; Elsevier: Amsterdam, The Netherlands, 2014; Volume 47, pp. 39–87. ISBN 0065-2806. [Google Scholar]
  34. Berry, C.; O’Neil, S.; Ben-Dov, E.; Jones, A.F.; Murphy, L.; Quail, M.A.; Holden, M.T.; Harris, D.; Zaritsky, A.; Parkhill, J. Complete Sequence and Organization of PBtoxis, the Toxin-Coding Plasmid of Bacillus thuringiensis subsp. israelensis. Appl. Environ. Microbiol. 2002, 68, 5082–5095. [Google Scholar] [CrossRef]
  35. Wu, J.; Wei, L.; He, J.; Fu, K.; Li, X.; Jia, L.; Wang, R.; Zhang, W. Characterization of a Novel Bacillus thuringiensis Toxin Active against Aedes Aegypti Larvae. Acta Trop. 2021, 223, 106088. [Google Scholar] [CrossRef]
  36. Palma, L.; Muñoz, D.; Berry, C.; Murillo, J.; Caballero, P. Bacillus thuringiensis Toxins: An Overview of Their Biocidal Activity. Toxins 2014, 6, 3296–3325. [Google Scholar] [CrossRef] [PubMed]
  37. Baumann, L.; Broadwell, A.H.; Baumann, P. Sequence Analysis of the Mosquitocidal Toxin Genes Encoding 51.4-and 41.9-Kilodalton Proteins from Bacillus sphaericus 2362 and 2297. J. Bacteriol. 1988, 170, 2045–2050. [Google Scholar] [CrossRef] [PubMed]
  38. El-Bendary, M.; Priest, F.G.; Charles, J.-F.; Mitchell, W.J. Crystal Protein Synthesis Is Dependent on Early Sporulation Gene Expression in Bacillus sphaericus. FEMS Microbiol. Lett. 2005, 252, 51–56. [Google Scholar] [CrossRef] [PubMed]
  39. Tangsongcharoen, C.; Chomanee, N.; Promdonkoy, B.; Boonserm, P. Lysinibacillus sphaericus Binary Toxin Induces Apoptosis in Susceptible Culex quinquefasciatus Larvae. J. Invertebr. Pathol. 2015, 128, 57–63. [Google Scholar] [CrossRef]
  40. Liu, J.-W.; Porter, A.G.; Wee, B.Y.; Thanabalu, T. New Gene from Nine Bacillus sphaericus Strains Encoding Highly Conserved 35.8-Kilodalton Mosquitocidal Toxins. Appl. Environ. Microbiol. 1996, 62, 2174–2176. [Google Scholar] [CrossRef]
  41. Jones, G.W.; Nielsen-Leroux, C.; Yang, Y.; Yuan, Z.; Fiuza Dumas, V.; Monnerat, R.G.; Berry, C. A New Cry Toxin with a Unique Two-component Dependency from Bacillus sphaericus. FASEB J. 2007, 21, 4112–4120. [Google Scholar] [CrossRef]
  42. Opota, O.; Gauthier, N.C.; Doye, A.; Berry, C.; Gounon, P.; Lemichez, E.; Pauron, D. Bacillus sphaericus Binary Toxin Elicits Host Cell Autophagy as a Response to Intoxication. PLoS ONE 2011, 6, e14682. [Google Scholar] [CrossRef]
  43. Filha, M.H.N.L.S.; Berry, C.; Regis, L. Lysinibacillus sphaericus: Toxins and Mode of Action, Applications for Mosquito Control and Resistance Management. In Advances in Insect Physiology; Elsevier: Amsterdam, The Netherlands, 2014; Volume 47, pp. 89–176. ISBN 0065-2806. [Google Scholar]
  44. Wirth, M.C.; Berry, C.; Walton, W.E.; Federici, B.A. Mtx Toxins from Lysinibacillus sphaericus Enhance Mosquitocidal Cry-Toxin Activity and Suppress Cry-Resistance in Culex quinquefasciatus. J. Invertebr. Pathol. 2014, 115, 62–67. [Google Scholar] [CrossRef]
  45. de Melo, J.V.; Jones, G.W.; Berry, C.; Vasconcelos, R.H.T.; de Oliveira, C.M.F.; Furtado, A.F.; Peixoto, C.A.; Silva-Filha, M.H.N.L. Cytopathological Effects of Bacillus sphaericus Cry48Aa/Cry49Aa Toxin on Binary Toxin-Susceptible and-Resistant Culex quinquefasciatus Larvae. Appl. Environ. Microbiol. 2009, 75, 4782–4789. [Google Scholar] [CrossRef]
  46. Darriet, F.; Duchon, S.; Hougard, J.M. Spinosad: A New Larvicide against Insecticide-Resistant Mosquito Larvae. J. Am. Mosq. Control Assoc. 2005, 21, 495–496. [Google Scholar] [CrossRef] [PubMed]
  47. Dripps, J.E.; Boucher, R.E.; Chloridis, A.; Cleveland, C.B.; DeAmicis, C.V.; Gomez, L.E.; Paroonagian, D.L.; Pavan, L.A.; Sparks, T.C.; Watson, G.B. The spinosyn insecticides. In Green Trends in Insect Control; López, O., Fernández-Bolaños, J.G., Eds.; Royal Society of Chemistry: London, UK, 2011; pp. 163–212. [Google Scholar]
  48. Chio, E.H.; Li, Q.X. Pesticide Research and Development: General Discussion and Spinosad Case. J. Agric. Food Chem. 2022, 70, 8913–8919. [Google Scholar] [CrossRef] [PubMed]
  49. Salgado, V.L. Studies on the mode of action of spinosad: Insect symptoms and physiological correlates. Pestic. Biochem. Physiol. 1998, 60, 91–102. [Google Scholar] [CrossRef]
  50. Vartoukian, S.R.; Palmer, R.M.; Wade, W.G. Strategies for Culture of ‘Unculturable’ Bacteria. FEMS Microbiol. Lett. 2010, 309, 1–7. [Google Scholar] [CrossRef]
  51. Falqueto, S.A.; Pitaluga, B.F.; de Sousa, J.R.; Targanski, S.K.; Campos, M.G.; de Oliveira Mendes, T.A.; da Silva, G.F.; Silva, D.H.S.; Soares, M.A. Bacillus spp. Metabolites Are Effective in Eradicating Aedes aegypti (Diptera: Culicidae) Larvae with Low Toxicity to Non-Target Species. J. Invertebr. Pathol. 2021, 179, 107525. [Google Scholar] [CrossRef] [PubMed]
  52. Katak, R.M.; Rocha, E.M.; Oliveira, J.C.; Muniz, V.A.; Oliveira, M.R.; Ferreira, F.A.; Silva, W.R.; Roque, R.A.; de Souza, A.Q.; Souza-Neto, J.A. Larvicidal Activities against Aedes aegypti of Supernatant and Pellet Fractions from Cultured Bacillus spp. Isolated from Amazonian Microenvironments. Trop. Med. Infect. Dis. 2021, 6, 104. [Google Scholar] [CrossRef] [PubMed]
  53. Susetyo, R.D.; Nafidiastri, F.A.; Zain, R.A.; Sari, R.P.; Geraldi, A. Potential Biocontrol Agent of Indigenous Bacillus sp. EG6. 4: Molecular Identification, Larvicidal Toxicity, and Mechanism of Actions. Biodiversitas 2022, 23, 5431–5438. [Google Scholar]
  54. Maldonado, B.M.G.; Galan, W.L.J.; Rodriguez, P.C.; Quiroz, M.H. Evaluation of Polymer-Based Granular Formulations of Bacillus thuringiensis israelensis against Larval Aedes aegypti in the Laboratory. J Am. Mosq. Control Assoc. 2002, 18, 352–358. [Google Scholar]
  55. Armengol, G.; Hernandez, J.; Velez, J.G.; Orduz, S. Long-Lasting Effects of a Bacillus thuringiensis serovar israelensis Experimental Tablet Formulation for Aedes aegypti (Diptera: Culicidae) Control. J. Econ. Entomol. 2006, 99, 1590–1595. [Google Scholar] [CrossRef]
  56. de Araujo, A.P.; de Melo-Santos, M.A.V.; de Oliveira Carlos, S.; Rios, E.M.M.M.; Regis, L. Evaluation of an Experimental Product Based on Bacillus thuringiensis sorovar. israelensis against Aedes aegypti Larvae (Diptera: Culicidae). Biol. Control 2007, 41, 339–347. [Google Scholar] [CrossRef]
  57. de Melo-Santos, M.A.V.; de Araújo, A.P.; Rios, E.M.M.; Regis, L. Long Lasting Persistence of Bacillus thuringiensis serovar. israelensis Larvicidal Activity in Aedes aegypti (Diptera: Culicidae) Breeding Places Is Associated to Bacteria Recycling. Biol. Control 2009, 49, 186–191. [Google Scholar] [CrossRef]
  58. Ritchie, S.A.; Rapley, L.P.; Benjamin, S. Bacillus thuringiensis var. israelensis (Bti) Provides Residual Control of Aedes aegypti in Small Containers. Am. J. Trop. Med. Hyg. 2010, 82, 1053. [Google Scholar] [CrossRef]
  59. Kovendan, K.; Murugan, K.; Vincent, S.; Kamalakannan, S. Larvicidal Efficacy of Jatropha Curcas and Bacterial Insecticide, Bacillus thuringiensis, against Lymphatic Filarial Vector, Culex quinquefasciatus Say (Diptera: Culicidae). Parasitol. Res. 2011, 109, 1251–1257. [Google Scholar] [CrossRef] [PubMed]
  60. Zahran, H.E.-D.M.; Kawanna, M.A.; Bosly, H.A. Larvicidal Activity and Joint Action Toxicity of Certain Combating Agents on Culex Pipiens L. Mosquitoes. Annu. Res. Rev. Biol. 2013, 3, 1055–1065. [Google Scholar]
  61. Bideshi, D.K.; Waldrop, G.; Fernandez-Luna, M.T.; Diaz-Mendoza, M.; Wirth, M.C.; Johnson, J.J.; Park, H.-W.; Federici, B.A. Intermolecular Interaction between Cry2Aa and Cyt1Aa and Its Effect on Larvicidal Activity against Culex quinquefasciatus. J. Microbiol. Biotechnol. 2013, 23, 1107–1115. [Google Scholar] [CrossRef] [PubMed]
  62. Ermolova, V.P.; Grishechkina, S.D.; Belousova, M.E.; Antonets, K.S.; Nizhnikov, A.A. Insecticidal Properties of Bacillus thuringiensis var. israelensis. II. Comparative Morphological and Molecular Genetic Analysis of the Crystallogenic and Acrystallogenic Strains. Sel’skokhozyaistvennaya Biol. 2019, 54, 1281–1289. [Google Scholar] [CrossRef]
  63. Valtierra-de-Luis, D.; Villanueva, M.; Lai, L.; Williams, T.; Caballero, P. Potential of Cry10Aa and Cyt2Ba, Two Minority δ-Endotoxins Produced by Bacillus thuringiensis ser. israelensis, for the Control of Aedes aegypti Larvae. Toxins 2020, 12, 355. [Google Scholar] [CrossRef]
  64. Nasser, S.; da Costa, M.P.M.; de Mello Ferreira, I.L.; Lima, J.B.P. K-Carrageenan-Bacillus thuringiensis israelensis Hydrogels: A Promising Material to Combat Larvae of the Aedes aegypti Mosquito. Carbohydr. Polym. Technol. Appl. 2021, 2, 100125. [Google Scholar] [CrossRef]
  65. Fernández-Chapa, D.; Luna-Olvera, H.A.; Ramirez-Villalobos, J.; Rojas-Verde, G.; Arévalo-Niño, K.; Galán-Wong, L.J. Viability and Reconstitution of Delta-Endotoxins from Bacillus thuringiensis var. israelensis Extracts after Forty Years of Storage against Aedes aegypti (Diptera: Culicidae). Egypt. J. Biol. Pest Control 2021, 31, 45. [Google Scholar] [CrossRef]
  66. Gad, A.A.; Al-Dakhil, A.A. Efficacy of Bacillus thuringiensis israelensis (Bti) and Four Plant Extracts on the Mortality and Development of Culex quinquefasciatus Say (Diptera: Cullicidae). Egypt. J. Biol. Pest Control 2018, 28, 62. [Google Scholar] [CrossRef]
  67. Shililu, J.I.; Tewolde, G.M.; Brantly, E.; Githure, J.I.; Mbogo, C.M.; Beier, J.C.; Fusco, R.; Novak, R.J. Efficacy of Bacillus thuringiensis israelensis, Bacillus sphaericus and Temephos for Managing Anopheles Larvae in Eritrea. J. Am. Mosq. Control Assoc. 2003, 19, 251–258. [Google Scholar] [PubMed]
  68. Pires, S.; Alves, J.; Dia, I.; Gomez, L.F. Susceptibility of Mosquito Vectors of the City of Praia, Cabo Verde, to Temephos and Bacillus thuringiensis var israelensis. PLoS ONE 2020, 15, e0234242. [Google Scholar] [CrossRef] [PubMed]
  69. Derua, Y.A.; Kweka, E.J.; Kisinza, W.N.; Yan, G.; Githeko, A.K.; Mosha, F.W. The Effect of Coexistence between Larvae of Anopheles gambiae and Culex quinquefasciatus on Larvicidal Efficacy of Bacillus thuringiensis var. israelensis. E. Afr. Sci. 2021, 3, 77–85. [Google Scholar] [CrossRef]
  70. Kroeger, A.; Horstick, O.; Riedl, C.; Kaiser, A.; Becker, N. The Potential for Malaria Control with the Biological Larvicide Bacillus thuringiensis israelensis (Bti) in Peru and Ecuador. Acta Trop. 1995, 60, 47–57. [Google Scholar] [CrossRef] [PubMed]
  71. Nartey, R.; Owusu-Dabo, E.; Kruppa, T.; Baffour-Awuah, S.; Annan, A.; Oppong, S.; Becker, N.; Obiri-Danso, K. Use of Bacillus thuringiensis var israelensis as a Viable Option in an Integrated Malaria Vector Control Programme in the Kumasi Metropolis, Ghana. Parasites Vectors 2013, 6, 116. [Google Scholar] [CrossRef]
  72. Dambach, P.; Louis, V.R.; Kaiser, A.; Ouedraogo, S.; Sié, A.; Sauerborn, R.; Becker, N. Efficacy of Bacillus thuringiensis var. israelensis against Malaria Mosquitoes in Northwestern Burkina Faso. Parasites Vectors 2014, 7, 371. [Google Scholar] [CrossRef]
  73. Demissew, A.; Balkew, M.; Girma, M. Larvicidal Activities of Chinaberry, Neem and Bacillus thuringiensis israelensis (Bti) to an Insecticide Resistant Population of Anopheles arabiensis from Tolay, Southwest Ethiopia. Asian Pac. J. Trop. Biomed. 2016, 6, 554–561. [Google Scholar] [CrossRef]
  74. Dambach, P.; Winkler, V.; Bärnighausen, T.; Traoré, I.; Ouedraogo, S.; Sié, A.; Sauerborn, R.; Becker, N.; Louis, V.R. Biological Larviciding against Malaria Vector Mosquitoes with Bacillus thuringiensis israelensis (Bti)–Long Term Observations and Assessment of Repeatability during an Additional Intervention Year of a Large-Scale Field Trial in Rural Burkina Faso. Glob. Health Action 2020, 13, 1829828. [Google Scholar] [CrossRef]
  75. Monnerat, R.G.; Dias, D.G.S.; da Silva, S.F.; Martins, E.S.; Berry, C.; Falcão, R.; Gomes, A.C.M.M.; Praça, L.B.; Soares, C.M.S. Screening of Bacillus thuringiensis Strains Effective against Mosquitoes. Pesqui. Agropecu. Bras. 2005, 40, 103–106. [Google Scholar] [CrossRef]
  76. Patil, C.D.; Patil, S.V.; Salunke, B.K.; Salunkhe, R.B. Insecticidal Potency of Bacterial Species Bacillus thuringiensis SV2 and Serratia Nematodiphila SV6 against Larvae of Mosquito Species Aedes aegypti, Anopheles stephensi, and Culex quinquefasciatus. Parasitol. Res. 2012, 110, 1841–1847. [Google Scholar] [CrossRef]
  77. Soares-da-Silva, J.; Pinheiro, V.C.S.; Litaiff-Abreu, E.; Polanczyk, R.A.; Tadei, W.P. Isolation of Bacillus thuringiensis from the State of Amazonas, in Brazil, and Screening against Aedes aegypti (Diptera, Culicidae). Rev. Bras. Entomol. 2015, 59, 01–06. [Google Scholar] [CrossRef]
  78. Soares-da-Silva, J.; Queirós, S.G.; de Aguiar, J.S.; Viana, J.L.; dos RAV Neta, M.; da Silva, M.C.; Pinheiro, V.C.; Polanczyk, R.A.; Carvalho-Zilse, G.A.; Tadei, W.P. Molecular Characterization of the Gene Profile of Bacillus Thuringiensis Berliner Isolated from Brazilian Ecosystems and Showing Pathogenic Activity against Mosquito Larvae of Medical Importance. Acta Trop. 2017, 176, 197–205. [Google Scholar] [CrossRef] [PubMed]
  79. Fatima, N.; Bibi, Z.; Rehman, A.; Bukhari, D.A. Biotoxicity Comparison of Bacillus Thuringiensis to Control Vector Borne Diseases against Mosquito Fauna. Saudi J. Biol. Sci. 2023, 30, 103610. [Google Scholar] [CrossRef] [PubMed]
  80. López-Molina, S.; do Nascimento, N.A.; Silva-Filha, M.H.N.L.; Guerrero, A.; Sánchez, J.; Pacheco, S.; Gill, S.S.; Soberón, M.; Bravo, A. In Vivo Nanoscale Analysis of the Dynamic Synergistic Interaction of Bacillus Thuringiensis Cry11Aa and Cyt1Aa Toxins in Aedes Aegypti. PLoS Pathog. 2021, 17, e1009199. [Google Scholar] [CrossRef] [PubMed]
  81. Roy, M.; Chatterjee, S.; Dangar, T.K. Characterization and Mosquitocidal Potency of a Bacillus Thuringiensis Strain of Rice Field Soil of Burdwan, West Bengal, India. Microb. Pathog. 2021, 158, 105093. [Google Scholar] [CrossRef]
  82. Bernal, L.; Dussán, J. Synergistic Effect of Lysinibacillus sphaericus and Glyphosate on Temephos-Resistant Larvae of Aedes aegypti. Parasites Vectors 2020, 13, 68. [Google Scholar] [CrossRef]
  83. Almeida, J.; Mohanty, A.; Dharini, N.; Hoti, S.L.; Kerkar, S.; Kumar, A. A Report on Novel Mosquito Pathogenic Bacillus spp. Isolated from a Beach in Goa, India. Int. J. Mosq. Res. 2020, 7, 21–29. [Google Scholar]
  84. Nicolas, L.; Dossou-Yovo, J. Differential Effects of Bacillus sphaericus Strain 2362 on Culex quinquefasciatus and Its Competitor Culex cinereus in West Africa. Med. Vet. Entomol. 1987, 1, 23–27. [Google Scholar] [CrossRef] [PubMed]
  85. Andrade, C.; Campos, J.; Cabrini, I.; Filho, C.; Hibi, S. Susceptibilidade de Populações de Culex quinquefasciatus Say (Diptera: Culicidae) Sujeitas Ao Controle Com Bacillus sphaericus Neide No Rio Pinheiros, São Paulo. BioAssay 2009, 2, 1–4. [Google Scholar] [CrossRef]
  86. Lozano, L.C.; Ayala, J.A.; Dussán, J. Lysinibacillus Sphaericus S-Layer Protein Toxicity against Culex quinquefasciatus. Biotechnol. Lett. 2011, 33, 2037–2041. [Google Scholar] [CrossRef]
  87. Kale, A.; Hire, R.S.; Hadapad, A.B.; D’Souza, S.F.; Kumar, V. Interaction between Mosquito-Larvicidal Lysinibacillus sphaericus Binary Toxin Components: Analysis of Complex Formation. Insect Biochem. Mol. Biol. 2013, 43, 1045–1054. [Google Scholar] [CrossRef] [PubMed]
  88. Iftikhar, S.; Riaz, M.A.; Majeed, M.Z.; Afzal, M.; Ali, A.; Saadia, M.; Ali, Z.; Ahmed, S. Isolation, Characterization and Larvicidal Potential of Indigenous Soil Inhabiting Bacteria against Larvae of Southern House Mosquito (Culex quinquefasciatus Say). Int. J. Trop. Insect Sci. 2023, 43, 781–791. [Google Scholar] [CrossRef]
  89. Allievi, M.C.; Palomino, M.M.; Prado Acosta, M.; Lanati, L.; Ruzal, S.M.; Sánchez-Rivas, C. Contribution of S-Layer Proteins to the Mosquitocidal Activity of Lysinibacillus sphaericus. PLoS ONE 2014, 9, e111114. [Google Scholar] [CrossRef] [PubMed]
  90. Lee, H.L.; David, L.; Nazni, W.A.; Rozilawati, H.; Nurulhusna, H.; Afizah, A.N.; Rosilawati, R.; Roziah, A.; Teh, C.H.; Seleena, B. Thermally Applied Lysinibacillus sphaericus And Pyrethroids Against Culex sitiens Wiedemann And Culex quinquefasciatus Say In Malaysia. Southeast Asian J. Trop. Med. Public Health 2016, 47, 747–758. [Google Scholar]
  91. Guo, Q.-Y.; Hu, X.-M.; Cai, Q.-X.; Yan, J.-P.; Yuan, Z.-M. Interaction of Lysinibacillus sphaericus Cry48Aa/Cry49Aa Toxin with Midgut Brush-border Membrane Fractions from Culex cuinquefasciatus Larvae. Insect Mol. Biol. 2016, 25, 163–170. [Google Scholar] [CrossRef]
  92. Lozano, L.C.; Dussán, J. Synergistic Activity between S-Layer Protein and Spore–Crystal Preparations from Lysinibacillus sphaericus against Culex quinquefasciatus Larvae. Curr. Microbiol. 2017, 74, 371–376. [Google Scholar] [CrossRef]
  93. Karch, S.; Asidi, N.; Manzambi, Z.M.; Salaun, J.J. Efficacy of Bacillus sphaericus against the Malaria Vector Anopheles gambiae and Other Mosquitoes in Swamps and Rice Fields in Zaire. J. Am. Mosq. Control Assoc. 1992, 8, 376–380. [Google Scholar]
  94. Rodrigues, I.B.; Tadei, W.P.; Dias, J.M.C.d.S. Larvicidal Activity of Bacillus sphaericus 2362 against Anopheles nuneztovari, Anopheles darlingi and Anopheles braziliensis (Diptera, Culicidae). Rev. Inst. Med. Trop. São Paulo 1999, 41, 101–105. [Google Scholar] [CrossRef]
  95. Galardo, A.K.R.; Zimmerman, R.; Galardo, C.D. Larval Control of Anopheles (Nyssorhinchus) darlingi Using Granular Formulation of Bacillus sphaericus in Abandoned Gold-Miners Excavation Pools in the Brazilian Amazon Rainforest. Rev. Soc. Bras. Med. Trop. 2013, 46, 172–177. [Google Scholar] [CrossRef]
  96. Riaz, M.A.; Adang, M.J.; Hua, G.; Rezende, T.M.T.; Rezende, A.M.; Shen, G.-M. Identification of Lysinibacillus sphaericus Binary Toxin Binding Proteins in a Malarial Mosquito Cell Line by Proteomics: A Novel Approach towards Improving Mosquito Control. J. Proteom. 2020, 227, 103918. [Google Scholar] [CrossRef]
  97. Dhayalan, A.; Kannupaiyan, J.; Govindasamy, B.; Pachiappan, P. Extraction and Characterization of Secondary Metabolites from the Soil Bacterium, Acidovorax sp. SA5 and Evaluation of Their Larvicidal Activity against Aedes aegypti. Int. J. Environ. Res. 2019, 13, 47–58. [Google Scholar] [CrossRef]
  98. Das, D.; Chatterjee, S.; Dangar, T.K. Characterization and Mosquitocidal Potential of the Soil Bacteria Aneurinibacillus aneurinilyticus Isolated from Burdwan, West Bengal, India. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci. 2016, 86, 707–713. [Google Scholar] [CrossRef]
  99. Geetha, I.; Aruna, R.; Manonmani, A.M. Mosquitocidal Bacillus amyloliquefaciens: Dynamics of Growth & Production of Novel Pupicidal Biosurfactant. Indian J. Med. Res. 2014, 140, 427. [Google Scholar] [PubMed]
  100. Darriet, F.; Hougard, J.-M. An Isolate of Bacillus circulans Toxic to Mosquito Larvae. J. Am. Mosq. Control Assoc. Mosq. News 2002, 18, 65–67. [Google Scholar]
  101. Abinaya, M.; Vaseeharan, B.; Divya, M.; Vijayakumar, S.; Govindarajan, M.; Alharbi, N.S.; Khaled, J.M.; Al-Anbr, M.N.; Benelli, G. Structural Characterization of Bacillus licheniformis Dahb1 Exopolysaccharide—Antimicrobial Potential and Larvicidal Activity on Malaria and Zika Virus Mosquito Vectors. Environ. Sci. Pollut. Res. 2018, 25, 18604–18619. [Google Scholar] [CrossRef] [PubMed]
  102. Favret, M.E.; Yousten, A.A. Insecticidal Activity of Bacillus laterosporus. J. Invertebr. Pathol. 1985, 45, 195–203. [Google Scholar] [CrossRef]
  103. Ruiu, L.; Floris, I.; Satta, A.; Ellar, D.J. Toxicity of a Brevibacillus laterosporus Strain Lacking Parasporal Crystals against Musca Domestica and Aedes aegypti. Biol. Control 2007, 43, 136–143. [Google Scholar] [CrossRef]
  104. Zubasheva, M.V.; Ganushkina, L.A.; Smirnova, T.A.; Azizbekyan, R.R. Larvicidal Activity of Crystal-Forming Strains of Brevibacillus laterosporus. Appl. Biochem. Microbiol. 2010, 46, 755–762. [Google Scholar] [CrossRef]
  105. Barbieri, G.; Ferrari, C.; Mamberti, S.; Gabrieli, P.; Castelli, M.; Sassera, D.; Ursino, E.; Scoffone, V.C.; Radaelli, G.; Clementi, E. Identification of a Novel Brevibacillus laterosporus Strain With Insecticidal Activity Against Aedes albopictus Larvae. Front. Microbiol. 2021, 12, 624014. [Google Scholar] [CrossRef]
  106. Bedini, S.; Conti, B.; Hamze, R.; Muniz, E.R.; Fernandes, É.K.; Ruiu, L. Lethal and Sub-Lethal Activity of Brevibacillus laterosporus on the Mosquito Aedes albopictus and Side Effects on Non-Target Water-Dwelling Invertebrates. J. Invertebr. Pathol. 2021, 184, 107645. [Google Scholar] [CrossRef]
  107. Das, K.; Mukherjee, A.K. Assessment of Mosquito Larvicidal Potency of Cyclic Lipopeptides Produced by Bacillus subtilis Strains. Acta Trop. 2006, 97, 168–173. [Google Scholar] [CrossRef] [PubMed]
  108. Geetha, I.; Manonmani, A.M. Surfactin: A Novel Mosquitocidal Biosurfactant Produced by Bacillus subtilis ssp. subtilis (VCRC B471) and Influence of Abiotic Factors on Its Pupicidal Efficacy. Lett. Appl. Microbiol. 2010, 51, 406–412. [Google Scholar] [CrossRef] [PubMed]
  109. Ramathilaga, A.; Murugesan, A.G.; Prabu, C.S. Biolarvicidal Activity of Peanibacillus macerans and Bacillus subtilis Isolated from the Dead Larvae against Aedes aegypti-Vector for Chikungunya. Proc. Int. Acad. Ecol. Environ. Sci. 2012, 2, 90. [Google Scholar]
  110. Geetha, I.; Paily, K.P.; Manonmani, A.M. Mosquito Adulticidal Activity of a Biosurfactant Produced by Bacillus subtilis subsp. subtilis. Pest Manag. Sci. 2012, 68, 1447–1450. [Google Scholar] [CrossRef]
  111. Parthipan, P.; Sarankumar, R.K.; Jaganathan, A.; Amuthavalli, P.; Babujanarthanam, R.; Rahman, P.K.; Murugan, K.; Higuchi, A.; Benelli, G.; Rajasekar, A. Biosurfactants Produced by Bacillus subtilis A1 and Pseudomonas stutzeri NA3 Reduce Longevity and Fecundity of Anopheles stephensi and Show High Toxicity against Young Instars. Environ. Sci. Pollut. Res. 2018, 25, 10471–10481. [Google Scholar] [CrossRef]
  112. Dahmana, H.; Sambou, M.; Raoult, D.; Fenollar, F.; Mediannikov, O. Biological Control of Aedes albopictus: Obtained from the New Bacterial Candidates with Insecticidal Activity. Insects 2020, 11, 403. [Google Scholar] [CrossRef]
  113. Pradhan, A.K.; Rath, A.; Pradhan, N.; Hazra, R.K.; Nayak, R.R.; Kanjilal, S. Cyclic Lipopeptide Biosurfactant from Bacillus tequilensis Exhibits Multifarious Activity. 3 Biotech 2018, 8, 261. [Google Scholar] [CrossRef]
  114. Ramirez, J.L.; Short, S.M.; Bahia, A.C.; Saraiva, R.G.; Dong, Y.; Kang, S.; Tripathi, A.; Mlambo, G.; Dimopoulos, G. Chromobacterium Csp_P Reduces Malaria and Dengue Infection in Vector Mosquitoes and Has Entomopathogenic and in Vitro Anti-Pathogen Activities. PLoS Pathog. 2014, 10, e1004398. [Google Scholar] [CrossRef]
  115. Short, S.M.; Van Tol, S.; MacLeod, H.J.; Dimopoulos, G. Hydrogen Cyanide Produced by the Soil Bacterium Chromobacterium sp. Panama Contributes to Mortality in Anopheles Gambiae Mosquito Larvae. Sci. Rep. 2018, 8, 8358. [Google Scholar] [CrossRef]
  116. Gnambani, E.J.; Bilgo, E.; Dabiré, R.K.; Belem, A.M.G.; Diabaté, A. Infection of the Malaria Vector Anopheles coluzzii with the Entomopathogenic Bacteria Chromobacterium anophelis sp. Nov. IRSSSOUMB001 Reduces Larval Survival and Adult Reproductive Potential. Malar. J. 2023, 22, 122. [Google Scholar] [CrossRef]
  117. Wilson, J.J.; Harimuralikrishnaa, T.; Sivakumar, T.; Mahendran, S.; Ponmanickam, P.; Thangaraj, R.; Sevarkodiyone, S.; Alharbi, N.S.; Kadaikunnan, S.; Venkidasamy, B. Biogenic Synthesis of Silver Nanoparticles Using Pantoea stewartii and Priestia aryabhattai and Their Antimicrobial, Larvicidal, Histopathological, and Biotoxicity Potential. Bioengineering 2023, 10, 248. [Google Scholar] [CrossRef]
  118. Contreras, E.; Masuyer, G.; Qureshi, N.; Chawla, S.; Dhillon, H.S.; Lee, H.L.; Chen, J.; Stenmark, P.; Gill, S.S. A Neurotoxin That Specifically Targets Anopheles Mosquitoes. Nat. Commun. 2019, 10, 2869. [Google Scholar] [CrossRef] [PubMed]
  119. Luiz Rosa da Silva, J.; Undurraga Schwalm, F.; Eugênio Silva, C.; da Costa, M.; Heermann, R.; Santos da Silva, O. Larvicidal and Growth-Inhibitory Activity of Entomopathogenic Bacteria Culture Fluids against Aedes aegypti (Diptera: Culicidae). J. Econ. Entomol. 2017, 110, 378–385. [Google Scholar] [PubMed]
  120. da Silva, O.S.; Prado, G.R.; da Silva, J.L.R.; Silva, C.E.; da Costa, M.; Heermann, R. Oral Toxicity of Photorhabdus luminescens and Xenorhabdus nematophila (Enterobacteriaceae) against Aedes aegypti (Diptera: Culicidae). Parasitol. Res. 2013, 112, 2891–2896. [Google Scholar] [CrossRef]
  121. Vitta, A.; Thimpoo, P.; Meesil, W.; Yimthin, T.; Fukruksa, C.; Polseela, R.; Mangkit, B.; Tandhavanant, S.; Thanwisai, A. Larvicidal Activity of Xenorhabdus and Photorhabdus Bacteria against Aedes aegypti and Aedes albopictus. Asian Pac. J. Trop. Biomed. 2018, 8, 31. [Google Scholar] [CrossRef]
  122. Patil, C.D.; Patil, S.V.; Salunke, B.K.; Salunkhe, R.B. Prodigiosin Produced by Serratia marcescens NMCC46 as a Mosquito Larvicidal Agent against Aedes aegypti and Anopheles stephensi. Parasitol. Res. 2011, 109, 1179–1187. [Google Scholar] [CrossRef] [PubMed]
  123. Suryawanshi, R.K.; Patil, C.D.; Borase, H.P.; Narkhede, C.P.; Salunke, B.K.; Patil, S.V. Mosquito Larvicidal and Pupaecidal Potential of Prodigiosin from Serratia marcescens and Understanding Its Mechanism of Action. Pestic. Biochem. Physiol. 2015, 123, 49–55. [Google Scholar] [CrossRef] [PubMed]
  124. Heu, K.; Romoli, O.; Schönbeck, J.C.; Ajenoe, R.; Epelboin, Y.; Kircher, V.; Houël, E.; Estevez, Y.; Gendrin, M. The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota. Front. Microbiol. 2021, 12, 645701. [Google Scholar] [CrossRef]
  125. Bond, J.G.; Marina, C.F.; Williams, T. The Naturally Derived Insecticide Spinosad Is Highly Toxic to Aedes and Anopheles Mosquito Larvae. Med. Vet. Entomol. 2004, 18, 50–56. [Google Scholar] [CrossRef]
  126. Romi, R.; Proietti, S.; Di Luca, M.; Cristofaro, M. Laboratory Evaluation of the Bioinsecticide Spinosad for Mosquito Control. J. Am. Mosq. Control Assoc. 2006, 22, 93–96. [Google Scholar] [CrossRef]
  127. Antonio, G.E.; Sanchez, D.; Williams, T.; Marina, C.F. Paradoxical Effects of Sublethal Exposure to the Naturally Derived Insecticide Spinosad in the Dengue Vector Mosquito, Aedes aegypti. Pest Manag. Sci. Former. Pestic. Sci. 2009, 65, 323–326. [Google Scholar] [CrossRef] [PubMed]
  128. Thavara, U.; Tawatsin, A.; Asavadachanukorn, P.; Mulla, M.S. Field Evaluation in Thailand of Spinosad, a Larvicide Derived from Brevibacillus laterosporus (Actinomycetales) against Aedes aegypti (L.) Larvae. Southeast Asian J. Trop. Med. Public Health 2009, 40, 235. [Google Scholar] [PubMed]
  129. Jiang, Y.; Mulla, M.S. Laboratory and Field Evaluation of Spinosad, a Biorational Natural Product, against Larvae of Culex Mosquitoes. J. Am. Mosq. Control Assoc. 2009, 25, 456–466. [Google Scholar] [CrossRef] [PubMed]
  130. Aarthi, N.; Murugan, K. Larvicidal and Repellent Activity of Vetiveria Zizanioides L, Ocimum Basilicum Linn and the Microbial Pesticide Spinosad against Malarial Vector, Anopheles stephensi Liston (Insecta: Diptera: Culicidae). J. Biopestic. 2010, 3, 199–204. [Google Scholar]
  131. Prabhu, K.; Murugan, K.; Nareshkumar, A.; Bragadeeswaran, S. Larvicidal and Pupicidal Activity of Spinosad against the Malarial Vector Anopheles stephensi. Asian Pac. J. Trop. Med. 2011, 4, 610–613. [Google Scholar] [CrossRef] [PubMed]
  132. Su, T.; Cheng, M.-L.; Thieme, J. Laboratory and Field Evaluation of Spinosad Formulation Natular T30 against Immature Culex Mosquitoes (Diptera: Culicidae). J. Med. Entomol. 2014, 51, 837–844. [Google Scholar] [CrossRef] [PubMed]
  133. Sadanandane, C.; Gunasekaran, K.; Doss, P.S.B.; Jambulingam, P. Field Evaluation of the Biolarvicide, Spinosad 20 per Cent Emulsifiable Concentrate in Comparison to Its 12 per Cent Suspension Concentrate Formulation against Culex quinquefasciatus, the Vector of Bancroftian Filariasis in India. Indian J. Med. Res. 2018, 147, 32. [Google Scholar] [CrossRef]
  134. Vijayan, V.; Balaraman, K. Metabolites of Fungi & Actinomycetes Active against Mosquito Larvae. Indian J. Med. Res. 1991, 93, 115–117. [Google Scholar]
  135. Darbro, J.M.; Graham, R.I.; Kay, B.H.; Ryan, P.A.; Thomas, M.B. Evaluation of Entomopathogenic Fungi as Potential Biological Control Agents of the Dengue Mosquito, Aedes aegypti (Diptera: Culicidae). Biocontrol Sci. Technol. 2011, 21, 1027–1047. [Google Scholar] [CrossRef]
  136. Blanford, S.; Jenkins, N.E.; Read, A.F.; Thomas, M.B. Evaluating the Lethal and Pre-Lethal Effects of a Range of Fungi against Adult Anopheles stephensi Mosquitoes. Malar. J. 2012, 11, 365. [Google Scholar] [CrossRef]
  137. Ramirez, J.L.; Muturi, E.J.; Dunlap, C.; Rooney, A.P. Strain-Specific Pathogenicity and Subversion of Phenoloxidase Activity in the Mosquito Aedes aegypti by Members of the Fungal Entomopathogenic Genus Isaria. Sci. Rep. 2018, 8, 9896. [Google Scholar] [CrossRef] [PubMed]
  138. Vivekanandhan, P.; Bedini, S.; Shivakumar, M.S. Isolation and Identification of Entomopathogenic Fungus from Eastern Ghats of South Indian Forest Soil and Their Efficacy as Biopesticide for Mosquito Control. Parasitol. Int. 2020, 76, 102099. [Google Scholar] [CrossRef] [PubMed]
  139. Pathan, E.K.; Ghormade, V.; Tupe, S.G.; Deshpande, M.V. Insect Pathogenic Fungi and Their Applications: An Indian Perspective. Prog. Mycol. Indian Perspect. 2021, 311–327. [Google Scholar] [CrossRef]
  140. Renuka, S.; Vani, H.C.; Alex, E. Entomopathogenic Fungi as a Potential Management Tool for the Control of Urban Malaria Vector, Anopheles stephensi (Diptera: Culicidae). J. Fungi 2023, 9, 223. [Google Scholar] [CrossRef]
  141. Scholte, E.-J.; Knols, B.G.; Samson, R.A.; Takken, W. Entomopathogenic Fungi for Mosquito Control: A Review. J. Insect Sci. 2004, 4, 19. [Google Scholar] [CrossRef]
  142. Kanzok, S.M.; Jacobs-Lorena, M. Entomopathogenic Fungi as Biological Insecticides to Control Malaria. Trends Parasitol. 2006, 22, 49–51. [Google Scholar] [CrossRef]
  143. Fang, W.; Azimzadeh, P.; Leger, R.J.S. Strain Improvement of Fungal Insecticides for Controlling Insect Pests and Vector-Borne Diseases. Curr. Opin. Microbiol. 2012, 15, 232–238. [Google Scholar] [CrossRef] [PubMed]
  144. Cafarchia, C.; Pellegrino, R.; Romano, V.; Friuli, M.; Demitri, C.; Pombi, M.; Benelli, G.; Otranto, D. Delivery and Effectiveness of Entomopathogenic Fungi for Mosquito and Tick Control: Current Knowledge and Research Challenges. Acta Trop. 2022, 234, 106627. [Google Scholar] [CrossRef]
  145. de Paula, A.R.; Brito, E.S.; Pereira, C.R.; Carrera, M.P.; Samuels, R.I. Susceptibility of Adult Aedes aegypti (Diptera: Culicidae) to Infection by Metarhizium anisopliae and Beauveria bassiana: Prospects for Dengue Vector Control. Biocontrol Sci. Technol. 2008, 18, 1017–1025. [Google Scholar] [CrossRef]
  146. Buckner, E.A.; Williams, K.F.; Marsicano, A.L.; Latham, M.D.; Lesser, C.R. Evaluating the Vector Control Potential of the In2Care® Mosquito Trap against Aedes aegypti and Aedes albopictus under Semifield Conditions in Manatee County, Florida. J. Am. Mosq. Control Assoc. 2017, 33, 193–199. [Google Scholar] [CrossRef]
  147. Howard, A.F.; N’guessan, R.; Koenraadt, C.J.; Asidi, A.; Farenhorst, M.; Akogbéto, M.; Thomas, M.B.; Knols, B.G.; Takken, W. The Entomopathogenic Fungus Beauveria bassiana Reduces Instantaneous Blood Feeding in Wild Multi-Insecticide-Resistant Culex quinquefasciatus Mosquitoes in Benin, West Africa. Parasites Vectors 2010, 3, 87. [Google Scholar] [CrossRef] [PubMed]
  148. García-Munguía, A.M.; Garza-Hernández, J.A.; Rebollar-Tellez, E.A.; Rodríguez-Pérez, M.A.; Reyes-Villanueva, F. Transmission of Beauveria bassiana from Male to Female Aedes aegypti Mosquitoes. Parasites Vectors 2011, 4, 24. [Google Scholar] [CrossRef] [PubMed]
  149. George, J.; Jenkins, N.E.; Blanford, S.; Thomas, M.B.; Baker, T.C. Malaria Mosquitoes Attracted by Fatal Fungus. PLoS ONE 2013, 8, e62632. [Google Scholar] [CrossRef] [PubMed]
  150. Valero-Jiménez, C.A.; van Kan, J.A.; Koenraadt, C.J.; Zwaan, B.J.; Schoustra, S.E. Experimental Evolution to Increase the Efficacy of the Entomopathogenic Fungus Beauveria bassiana against Malaria Mosquitoes: Effects on Mycelial Growth and Virulence. Evol. Appl. 2017, 10, 433–443. [Google Scholar] [CrossRef]
  151. Shoukat, R.F.; Zafar, J.; Shakeel, M.; Zhang, Y.; Freed, S.; Xu, X.; Jin, F. Assessment of Lethal, Sublethal, and Transgenerational Effects of Beauveria bassiana on the Demography of Aedes albopictus (Culicidae: Diptera). Insects 2020, 11, 178. [Google Scholar] [CrossRef]
  152. Veys-Behbahani, R.; Sharififard, M.; Dinparast-Djadid, N.; Shamsi, J.; Fakoorziba, M.R. Laboratory Evolution of the Entomopathogenic Fungus Beauveria bassiana against Anopheles stephensi Larvae (Diptera: Culicidae). Asian Pac. J. Trop. Dis. 2014, 4, S799–S802. [Google Scholar] [CrossRef]
  153. Bezalwar, P.; Gomashe, A.; Gulhane, P. Laboratory-Based Evaluation of the Potential of Beauveria bassiana Crude Metabolites for Mosquito Larvae. Annihilation 2014, 9, 15–20. [Google Scholar]
  154. Farida, B.; Sonia, H.; Hakima, M.-K.; Fatma, B.; Fatma, H. Histological Changes in the Larvae of the Domestic Mosquito Culex pipiens Treated with the Entomopathogenic Fungus Beauveria bassiana. Sci. Res. Essays 2018, 13, 1–10. [Google Scholar]
  155. US EPA (United States of America—Environmental Protection Agency). Biopesticide Active Ingredients. Available online: https://www.epa.gov/ingredients-used-pesticide-products/biopesticide-active-ingredients (accessed on 12 April 2023).
  156. ANVISA Listas de Ingredientes Ativos Com Uso Autorizado e Banidos no Brasil. Available online: https://www.gov.br/anvisa/pt-br/assuntos/noticias-anvisa/2017/listas-de-ingredientes-ativos-com-uso-autorizado-e-banidos-no-brasil (accessed on 20 March 2023).
  157. Zimmermann, G. The Entomopathogenic Fungus Metarhizium anisopliae and Its Potential as a Biocontrol Agent. Pestic. Sci. 1993, 37, 375–379. [Google Scholar] [CrossRef]
  158. Freimoser, F.M.; Screen, S.; Bagga, S.; Hu, G.; St Leger, R.J. Expressed Sequence Tag (EST) Analysis of Two Subspecies of Metarhizium anisopliae Reveals a Plethora of Secreted Proteins with Potential Activity in Insect Hosts. Microbiology 2003, 149, 239–247. [Google Scholar] [CrossRef]
  159. Schrank, A.; Vainstein, M.H. Metarhizium anisopliae Enzymes and Toxins. Toxicon 2010, 56, 1267–1274. [Google Scholar] [CrossRef] [PubMed]
  160. Choi, C.J.; Lee, J.Y.; Woo, R.M.; Shin, T.Y.; Gwak, W.S.; Woo, S.D. An Effective Entomopathogenic Fungus Metarhizium anisopliae for the Simultaneous Control of Aedes albopictus and Culex pipiens Mosquito Adults. J. Asia Pac. Entomol. 2020, 23, 585–590. [Google Scholar] [CrossRef]
  161. Scholte, E.-J.; Knols, B.G.; Takken, W. Infection of the Malaria Mosquito Anopheles gambiae with the Entomopathogenic Fungus Metarhizium anisopliae Reduces Blood Feeding and Fecundity. J. Invertebr. Pathol. 2006, 91, 43–49. [Google Scholar] [CrossRef] [PubMed]
  162. Pereira, C.R.; de Paula, A.R.; Gomes, S.A.; Pedra, P.C.O., Jr.; Samuels, R.I. The Potential of Metarhizium anisopliae and Beauveria bassiana Isolates for the Control of Aedes aegypti (Diptera: Culicidae) Larvae. Biocontrol Sci. Technol. 2009, 19, 881–886. [Google Scholar] [CrossRef]
  163. Koodalingam, A.; Dayanidhi, M.K. Studies on Biochemical and Synergistic Effects of Immunosuppressive Concentration of Imidacloprid with Beauveria bassiana and Metarhizium anisopliae for Enhancement of Virulence against Vector Mosquito Culex quinquefasciatus. Pestic. Biochem. Physiol. 2021, 176, 104882. [Google Scholar] [CrossRef]
  164. Butt, T.M.; Greenfield, B.P.; Greig, C.; Maffeis, T.G.; Taylor, J.W.; Piasecka, J.; Dudley, E.; Abdulla, A.; Dubovskiy, I.M.; Garrido-Jurado, I. Metarhizium anisopliae Pathogenesis of Mosquito Larvae: A Verdict of Accidental Death. PLoS ONE 2013, 8, e81686. [Google Scholar] [CrossRef]
  165. Jaber, S.; Mercier, A.; Knio, K.; Brun, S.; Kambris, Z. Isolation of Fungi from Dead Arthropods and Identification of a New Mosquito Natural Pathogen. Parasites Vectors 2016, 9, 491. [Google Scholar] [CrossRef]
  166. Soni, N.; Prakash, S. Aspergillus niger Metabolites Efficacies against the Mosquito Larval (Culex quinquefasciatus, Anopheles stephensi and Aedes aegypti) Population after Column Chromatography. Am. J. Microbiol. Res. 2011, 2, 15–20. [Google Scholar]
  167. Balumahendhiran, K.; Vivekanandhan, P.; Shivakumar, M.S. Mosquito Control Potential of Secondary Metabolites Isolated from Aspergillus flavus and Aspergillus fumigatus. Biocatal. Agric. Biotechnol. 2019, 21, 101334. [Google Scholar] [CrossRef]
  168. Baskar, K.; Chinnasamy, R.; Pandy, K.; Venkatesan, M.; Sebastian, P.J.; Subban, M.; Thomas, A.; Kweka, E.J.; Devarajan, N. Larvicidal and Histopathology Effect of Endophytic Fungal Extracts of Aspergillus tamarii against Aedes aegypti and Culex quinquefasciatus. Heliyon 2020, 6, e05331. [Google Scholar] [CrossRef]
  169. Vasantha-Srinivasan, P.; Karthi, S.; Chellappandian, M.; Ponsankar, A.; Thanigaivel, A.; Senthil-Nathan, S.; Chandramohan, D.; Ganesan, R. Aspergillus flavus (Link) Toxins Reduces the Fitness of Dengue Vector Aedes aegypti (Linn.) and Their Non-Target Toxicity against Aquatic Predator. Microb. Pathog. 2019, 128, 281–287. [Google Scholar] [CrossRef] [PubMed]
  170. Karthi, S.; Vasantha-Srinivasan, P.; Ganesan, R.; Ramasamy, V.; Senthil-Nathan, S.; Khater, H.F.; Radhakrishnan, N.; Amala, K.; Kim, T.-J.; El-Sheikh, M.A. Target Activity of Isaria tenuipes (Hypocreales: Clavicipitaceae) Fungal Strains against Dengue Vector Aedes aegypti (Linn.) and Its Non-Target Activity against Aquatic Predators. J. Fungi 2020, 6, 196. [Google Scholar] [CrossRef] [PubMed]
  171. Banu, A.N.; Balasubramanian, C. Optimization and Synthesis of Silver Nanoparticles Using Isaria fumosorosea against Human Vector Mosquitoes. Parasitol. Res. 2014, 113, 3843–3851. [Google Scholar] [CrossRef] [PubMed]
  172. Podder, D.; Ghosh, S.K. A New Application of Trichoderma asperellum as an Anopheline Larvicide for Eco Friendly Management in Medical Science. Sci. Rep. 2019, 9, 1108. [Google Scholar] [CrossRef] [PubMed]
  173. Mao, Z.; Wang, W.; Su, R.; Gu, G.; Liu, Z.L.; Lai, D.; Zhou, L. Hyalodendrins A and B, New Decalin-Type Tetramic Acid Larvicides from the Endophytic Fungus Hyalodendriella sp. Ponipodef12. Molecules 2019, 25, 114. [Google Scholar] [CrossRef] [PubMed]
  174. Kirsch, J.M.; Tay, J.-W. Larval Mortality and Ovipositional Preference in Aedes albopictus (Diptera: Culicidae) Induced by the Entomopathogenic Fungus Beauveria bassiana (Hypocreales: Cordycipitaceae). J. Med. Entomol. 2022, 59, 1687–1693. [Google Scholar] [CrossRef]
  175. Lee, J.Y.; Woo, R.M.; Choi, C.J.; Shin, T.Y.; Gwak, W.S.; Woo, S.D. Beauveria bassiana for the Simultaneous Control of Aedes albopictus and Culex pipiens Mosquito Adults Shows High Conidia Persistence and Productivity. AMB Express 2019, 9, 206. [Google Scholar] [CrossRef]
  176. Alves, S.B.; Alves, L.F.A.; Lopes, R.B.; Pereira, R.M.; Vieira, S.A. Potential of Some Metarhizium anisopliae Isolates for Control of Culex quinquefasciatus (Dipt., Culicidae). J. Appl. Entomol. 2002, 126, 504–509. [Google Scholar] [CrossRef]
  177. Scholte, E.-J.; Takken, W.; Knols, B.G. Infection of Adult Aedes aegypti and Ae. albopictus Mosquitoes with the Entomopathogenic Fungus Metarhizium anisopliae. Acta Trop. 2007, 102, 151–158. [Google Scholar] [CrossRef]
  178. Seye, F.; Ndiaye, M.; Faye, O.; Afoutou, J.M. Evaluation of Entomopathogenic Fungus Metarhizium anisopliae Formulated with Suneem (Neem Oil) against Anopheles gambiae Sl and Culex quinquefasciatus Adults. Malar. Chemother. Control Elimin. 2012, 1, 235494. [Google Scholar]
  179. Vivekanandhan, P.; Swathy, K.; Kalaimurugan, D.; Ramachandran, M.; Yuvaraj, A.; Kumar, A.N.; Manikandan, A.T.; Poovarasan, N.; Shivakumar, M.S.; Kweka, E.J. Larvicidal Toxicity of Metarhizium anisopliae Metabolites against Three Mosquito Species and Non-Targeting Organisms. PLoS ONE 2020, 15, e0232172. [Google Scholar] [CrossRef] [PubMed]
  180. Govindarajan, M.; Jebanesan, A.; Reetha, D. Larvicidal Effect of Extracellular Secondary Metabolites of Different Fungi against the Mosquito, Culex quinquefasciatus Say. Trop. Biomed. 2005, 22, 1–3. [Google Scholar] [PubMed]
  181. Ragavendran, C.; Natarajan, D. Insecticidal Potency of Aspergillus terreus against Larvae and Pupae of Three Mosquito Species Anopheles stephensi, Culex quinquefasciatus, and Aedes aegypti. Environ. Sci. Pollut. Res. 2015, 22, 17224–17237. [Google Scholar] [CrossRef] [PubMed]
  182. Chinnasamy, R.; Govindasamy, B.; Venkatesh, M.; Magudeeswaran, S.; Dhanarajan, A.; Devarajan, N.; Willie, P.; Perumal, V.; Mekchay, S.; Krutmuang, P. Bio-Efficacy of Insecticidal Molecule Emodin against Dengue, Filariasis, and Malaria Vectors. Environ. Sci. Pollut. Res. 2023, 30, 61842–61862. [Google Scholar] [CrossRef]
  183. Pinnock, D.E.; Garcia, R.; Cubbin, C.M. Beauveria tenella as a Control Agent for Mosquito Larvae. J. Invertebr. Pathol. 1973, 22, 143–147. [Google Scholar] [CrossRef] [PubMed]
  184. Ragavendran, C.; Balasubramani, G.; Tijo, C.; Manigandan, V.; Kweka, E.J.; Karthika, P.; Sivasankar, P.; Thomas, A.; Natarajan, D.; Nakouti, I. Cladophialophora bantiana Metabolites Are Efficient in the Larvicidal and Ovicidal Control of Aedes aegypti, and Culex quinquefasciatus and Have Low Toxicity in Zebrafish Embryo. Sci. Total Environ. 2022, 852, 158502. [Google Scholar] [CrossRef]
  185. Mohanty, S.S.; Prakash, S. Effects of Culture Media on Larvicidal Property of Secondary Metabolites of Mosquito Pathogenic Fungus Chrysosporium lobatum (Moniliales: Moniliaceae). Acta Trop. 2009, 109, 50–54. [Google Scholar] [CrossRef]
  186. Verma, P.; Prakash, S. Efficacy of Chrysosporium tropicum Metabolite against Mixed Population of Adult Mosquito (Culex quinquefasciatus, Anopheles stephensii, and Aedes aegypti) after Purification with Flash Chromatography. Parasitol. Res. 2010, 107, 163–166. [Google Scholar] [CrossRef]
  187. Pradeep, F.S.; Palaniswamy, M.; Ravi, S.; Thangamani, A.; Pradeep, B.V. Larvicidal Activity of a Novel Isoquinoline Type Pigment from Fusarium moniliforme KUMBF1201 against Aedes aegypti and Anopheles stephensi. Process Biochem. 2015, 50, 1479–1486. [Google Scholar] [CrossRef]
  188. Vivekanandhan, P.; Karthi, S.; Shivakumar, M.S.; Benelli, G. Synergistic Effect of Entomopathogenic Fungus Fusarium oxysporum Extract in Combination with Temephos against Three Major Mosquito Vectors. Pathog. Glob. Health 2018, 112, 37–46. [Google Scholar] [CrossRef]
  189. Ragavendran, C.; Mariappan, T.; Natarajan, D. Larvicidal, Histopathological Efficacy of Penicillium daleae against Larvae of Culex quinquefasciatus and Aedes aegypti plus Biotoxicity on Artemia Nauplii a Non-Target Aquatic Organism. Front. Pharmacol. 2017, 8, 773. [Google Scholar] [CrossRef]
  190. Saady, R.H.; Mansoor, A.J. Laboratory Evaluation of the Entomopathogenic Fungi Penicillium marneffei and Verticillium lecanii against Culex pipeins Molestus. Indian J. Forensic Med. Toxicol. 2021, 15, 2126–2133. [Google Scholar]
  191. Arunthirumeni, M.; Vinitha, G.; Shivakumar, M.S. Antifeedant and Larvicidal Activity of Bioactive Compounds Isolated from Entomopathogenic Fungi Penicillium sp. for the Control of Agricultural and Medically Important Insect Pest (Spodoptera Litura and Culex quinquefasciatus). Parasitol. Int. 2023, 92, 102688. [Google Scholar] [CrossRef] [PubMed]
  192. Ragavendran, C.; Manigandan, V.; Kamaraj, C.; Balasubramani, G.; Prakash, J.S.; Perumal, P.; Natarajan, D. Larvicidal, Histopathological, Antibacterial Activity of Indigenous Fungus Penicillium sp. against Aedes aegypti L and Culex quinquefasciatus (Say)(Diptera: Culicidae) and Its Acetylcholinesterase Inhibition and Toxicity Assessment of Zebrafish (Danio Rerio). Front. Microbiol. 2019, 10, 427. [Google Scholar] [PubMed]
  193. Bücker, A.; Bücker, N.C.F.; de Souza, A.Q.L.; da Gama, A.M.; Rodrigues-Filho, E.; da Costa, F.M.; Nunez, C.V.; Tadei, W.P. Larvicidal Effects of Endophytic and Basidiomycete Fungus Extracts on Aedes and Anopheles Larvae (Diptera, Culicidae). Rev. Soc. Bras. Med. Trop. 2013, 46, 411–419. [Google Scholar] [CrossRef]
  194. Matasyoh, J.C.; Dittrich, B.; Schueffler, A.; Laatsch, H. Larvicidal Activity of Metabolites from the Endophytic Podospora sp. against the Malaria Vector Anopheles gambiae. Parasitol. Res. 2011, 108, 561–566. [Google Scholar] [CrossRef] [PubMed]
  195. Sundaravadivelan, C.; Padmanabhan, M.N. Effect of Mycosynthesized Silver Nanoparticles from Filtrate of Trichoderma harzianum against Larvae and Pupa of Dengue Vector Aedes aegypti L. Environ. Sci. Pollut. Res. 2014, 21, 4624–4633. [Google Scholar] [CrossRef] [PubMed]
  196. Thiyagarajan, P.; Kumar, P.M.; Murugan, K.; Kovendan, K. Mosquito Larvicidal, Pupicidal and Field Evaluation of Microbial Insecticide, Verticillium lecanii against the Malarial Vector, Anopheles stephensi. Acta Biol. Indica 2014, 3, 541–548. [Google Scholar]
  197. Toghueo, R.M.K.; Kemgne, E.A.M.; Eke, P.; Kanko, M.I.M.; Dize, D.; Sahal, D.; Boyom, F.F. Antiplasmodial Potential and GC-MS Fingerprint of Endophytic Fungal Extracts Derived from Cameroonian Annona Muricata. J. Ethnopharmacol. 2019, 235, 111–121. [Google Scholar] [CrossRef]
  198. Hayibor, K.; Kwain, S.; Osei, E.; Nartey, A.P.; Tetevi, G.M.; Owusu, K.B.-A.; Camas, M.; Camas, A.S.; Kyeremeh, K. Ghanaian Mangrove Wetland Endophytic Fungus, Penicillium herquei Strain BRS2A-AR Produces (9Z, 11E)-13-Oxooctadeca-9, 11-Dienoic Acid with Activity against Trichomonas Mobilensis. Int. J. Biol. Chem. Sci. 2019, 13, 1918–1937. [Google Scholar] [CrossRef]
  199. Shi, Y.-N.; Pusch, S.; Shi, Y.-M.; Richter, C.; Maciá-Vicente, J.G.; Schwalbe, H.; Kaiser, M.; Opatz, T.; Bode, H.B. (±)-Alternarlactones A and B, Two Antiparasitic Alternariol-like Dimers from the Fungus Alternaria alternata P1210 Isolated from the Halophyte Salicornia sp. J. Org. Chem. 2019, 84, 11203–11209. [Google Scholar] [CrossRef]
  200. Cappelli, A.; Valzano, M.; Cecarini, V.; Bozic, J.; Rossi, P.; Mensah, P.; Amantini, C.; Favia, G.; Ricci, I. Killer Yeasts Exert Anti-Plasmodial Activities against the Malaria Parasite Plasmodium berghei in the Vector Mosquito Anopheles stephensi and in Mice. Parasites Vectors 2019, 12, 329. [Google Scholar] [CrossRef] [PubMed]
  201. Niu, G.; Wang, B.; Zhang, G.; King, J.B.; Cichewicz, R.H.; Li, J. Targeting Mosquito FREP1 with a Fungal Metabolite Blocks Malaria Transmission. Sci. Rep. 2015, 5, 14694. [Google Scholar] [CrossRef]
  202. Blanford, S.; Chan, B.H.; Jenkins, N.; Sim, D.; Turner, R.J.; Read, A.F.; Thomas, M.B. Fungal Pathogen Reduces Potential for Malaria Transmission. Science 2005, 308, 1638–1641. [Google Scholar] [CrossRef] [PubMed]
  203. Heinig, R.L.; Thomas, M.B. Interactions between a Fungal Entomopathogen and Malaria Parasites within a Mosquito Vector. Malar. J. 2015, 14, 103182. [Google Scholar] [CrossRef] [PubMed]
  204. Fang, W.; Vega-Rodríguez, J.; Ghosh, A.K.; Jacobs-Lorena, M.; Kang, A.; St. Leger, R.J. Development of Transgenic Fungi That Kill Human Malaria Parasites in Mosquitoes. Science 2011, 331, 1074–1077. [Google Scholar] [CrossRef]
  205. Dennison, N.J.; Jupatanakul, N.; Dimopoulos, G. The Mosquito Microbiota Influences Vector Competence for Human Pathogens. Curr. Opin. Insect Sci. 2014, 3, 6–13. [Google Scholar] [CrossRef]
  206. Carlson, J.S.; Short, S.M.; Angleró-Rodríguez, Y.I.; Dimopoulos, G. Larval Exposure to Bacteria Modulates Arbovirus Infection and Immune Gene Expression in Adult Aedes aegypti. Dev. Comp. Immunol. 2020, 104, 103540. [Google Scholar] [CrossRef]
  207. Gao, H.; Cui, C.; Wang, L.; Jacobs-Lorena, M.; Wang, S. Mosquito Microbiota and Implications for Disease Control. Trends Parasitol. 2020, 36, 98–111. [Google Scholar] [CrossRef]
  208. Gabrieli, P.; Caccia, S.; Varotto-Boccazzi, I.; Arnoldi, I.; Barbieri, G.; Comandatore, F.; Epis, S. Mosquito Trilogy: Microbiota, Immunity and Pathogens, and Their Implications for the Control of Disease Transmission. Front. Microbiol. 2021, 12, 630438. [Google Scholar] [CrossRef]
  209. Cansado-Utrilla, C.; Zhao, S.Y.; McCall, P.J.; Coon, K.L.; Hughes, G.L. The Microbiome and Mosquito Vectorial Capacity: Rich Potential for Discovery and Translation. Microbiome 2021, 9, 111. [Google Scholar] [CrossRef]
  210. Wang, J.; Gao, L.; Aksoy, S. Microbiota in Disease-Transmitting Vectors. Nat. Rev. Microbiol. 2023, 21, 604–618. [Google Scholar] [CrossRef]
  211. Douglas, A.E. Lessons from Studying Insect Symbioses. Cell Host Microbe 2011, 10, 359–367. [Google Scholar] [CrossRef]
  212. Minard, G.; Mavingui, P.; Moro, C.V. Diversity and Function of Bacterial Microbiota in the Mosquito Holobiont. Parasites Vectors 2013, 6, 146. [Google Scholar] [CrossRef] [PubMed]
  213. Kumar, A.; Srivastava, P.; Sirisena, P.; Dubey, S.K.; Kumar, R.; Shrinet, J.; Sunil, S. Mosquito Innate Immunity. Insects 2018, 9, 95. [Google Scholar] [CrossRef] [PubMed]
  214. Ferreira, Q.R.; Lemos, F.F.B.; Moura, M.N.; de Nascimento, J.O.S.; Novaes, A.F.; Barcelos, I.S.; Fernandes, L.A.; de Amaral, L.S.B.; Barreto, F.K.; de Melo, F.F. Role of the Microbiome in Aedes spp. Vector Competence: What Do We Know? Viruses 2023, 15, 779. [Google Scholar] [CrossRef]
  215. Saab, S.A.; Dohna, H.Z.; Nilsson, L.K.; Onorati, P.; Nakhleh, J.; Terenius, O.; Osta, M.A. The Environment and Species Affect Gut Bacteria Composition in Laboratory Co-Cultured Anopheles gambiae and Aedes albopictus Mosquitoes. Sci. Rep. 2020, 10, 3352. [Google Scholar] [CrossRef]
  216. Mosquera, K.D.; Nilsson, L.K.J.; de Oliveira, M.R.; Rocha, E.M.; Marinotti, O.; Håkansson, S.; Tadei, W.P.; de Souza, A.Q.L.; Terenius, O. Comparative Assessment of the Bacterial Communities Associated with Anopheles darlingi Immature Stages and Their Breeding Sites in the Brazilian Amazon. Parasites Vectors 2023, 16, 156. [Google Scholar] [CrossRef]
  217. Dos Santos, N.A.C.; de Carvalho, V.R.; Souza Neto, J.; Alonso, D.P.; Ribolla, P.E.M.; Medeiros, J.F.; da Araujo, M.S. Bacterial Microbiota from Lab-Reared and Field-Captured Anopheles darlingi Midgut and Salivary Gland. Microorganisms 2023, 11, 1145. [Google Scholar] [CrossRef] [PubMed]
  218. Dong, Y.; Manfredini, F.; Dimopoulos, G. Implication of the Mosquito Midgut Microbiota in the Defense against Malaria Parasites. PLoS Pathog. 2009, 5, e1000423. [Google Scholar] [CrossRef] [PubMed]
  219. Cirimotich, C.M.; Dong, Y.; Garver, L.S.; Sim, S.; Dimopoulos, G. Mosquito Immune Defenses against Plasmodium Infection. Dev. Comp. Immunol. 2010, 34, 387–395. [Google Scholar] [CrossRef]
  220. Wang, Y.; Gilbreath III, T.M.; Kukutla, P.; Yan, G.; Xu, J. Dynamic Gut Microbiome across Life History of the Malaria Mosquito Anopheles gambiae in Kenya. PLoS ONE 2011, 6, e24767. [Google Scholar] [CrossRef]
  221. Gendrin, M.; Christophides, G.K. The Anopheles Mosquito Microbiota and Their Impact on Pathogen Transmission. In Anopheles Mosquitoes-New Insights into Malaria Vectors; IntechOpen: Rijeka, Croatia, 2013; ISBN 953-51-1188-4. [Google Scholar]
  222. Ricci, I.; Valzano, M.; Ulissi, U.; Epis, S.; Cappelli, A.; Favia, G. Symbiotic Control of Mosquito Borne Disease. Pathog. Glob. Health 2012, 106, 380–385. [Google Scholar] [CrossRef]
  223. Eappen, A.G.; Smith, R.C.; Jacobs-Lorena, M. Enterobacter-Activated Mosquito Immune Responses to Plasmodium Involve Activation of SRPN6 in Anopheles stephensi. PLoS ONE 2013, 8, e62937. [Google Scholar]
  224. Romoli, O.; Gendrin, M. The Tripartite Interactions between the Mosquito, Its Microbiota and Plasmodium. Parasites Vectors 2018, 11, 200. [Google Scholar] [CrossRef]
  225. Shi, C.; Beller, L.; Wang, L.; Rosales Rosas, A.; De Coninck, L.; Héry, L.; Mousson, L.; Pagès, N.; Raes, J.; Delang, L. Bidirectional Interactions between Arboviruses and the Bacterial and Viral Microbiota in Aedes aegypti and Culex quinquefasciatus. MBio 2022, 13, e01021-22. [Google Scholar] [CrossRef]
  226. Pumpuni, C.B.; Beier, M.S.; Nataro, J.P.; Guers, L.D.; Davis, J.R. Plasmodium falciparum: Inhibition of Sporogonic Development in Anopheles stephensi by Gram-Negative Bacteria. Exp. Parasitol. 1993, 77, 195–199. [Google Scholar] [CrossRef]
  227. Cirimotich, C.M.; Dong, Y.; Clayton, A.M.; Sandiford, S.L.; Souza-Neto, J.A.; Mulenga, M.; Dimopoulos, G. Natural Microbe-Mediated Refractoriness to Plasmodium Infection in Anopheles gambiae. Science 2011, 332, 855–858. [Google Scholar] [CrossRef]
  228. Dennison, N.J.; Saraiva, R.G.; Cirimotich, C.M.; Mlambo, G.; Mongodin, E.F.; Dimopoulos, G. Functional Genomic Analyses of Enterobacter, Anopheles and Plasmodium Reciprocal Interactions That Impact Vector Competence. Malar. J. 2016, 15, 425. [Google Scholar] [CrossRef]
  229. Bando, H.; Okado, K.; Guelbeogo, W.M.; Badolo, A.; Aonuma, H.; Nelson, B.; Fukumoto, S.; Xuan, X.; Sagnon, N.; Kanuka, H. Intra-Specific Diversity of Serratia marcescens in Anopheles Mosquito Midgut Defines Plasmodium Transmission Capacity. Sci. Rep. 2013, 3, 1641. [Google Scholar] [CrossRef]
  230. Tchioffo, M.T.; Boissiere, A.; Churcher, T.S.; Abate, L.; Gimonneau, G.; Nsango, S.E.; Awono-Ambene, P.H.; Christen, R.; Berry, A.; Morlais, I. Modulation of Malaria Infection in Anopheles gambiae Mosquitoes Exposed to Natural Midgut Bacteria. PLoS ONE 2013, 8, e81663. [Google Scholar] [CrossRef]
  231. Bai, L.; Wang, L.; Vega-Rodríguez, J.; Wang, G.; Wang, S. A Gut Symbiotic Bacterium Serratia marcescens Renders Mosquito Resistance to Plasmodium Infection through Activation of Mosquito Immune Responses. Front. Microbiol. 2019, 10, 1580. [Google Scholar] [CrossRef]
  232. Gao, H.; Bai, L.; Jiang, Y.; Huang, W.; Wang, L.; Li, S.; Zhu, G.; Wang, D.; Huang, Z.; Li, X. A Natural Symbiotic Bacterium Drives Mosquito Refractoriness to Plasmodium Infection via Secretion of an Antimalarial Lipase. Nat. Microbiol. 2021, 6, 806–817. [Google Scholar] [CrossRef] [PubMed]
  233. Cappelli, A.; Damiani, C.; Mancini, M.V.; Valzano, M.; Rossi, P.; Serrao, A.; Ricci, I.; Favia, G. Asaia Activates Immune Genes in Mosquito Eliciting an Anti-Plasmodium Response: Implications in Malaria Control. Front. Genet. 2019, 10, 836. [Google Scholar] [CrossRef] [PubMed]
  234. Ramirez, J.L.; Souza-Neto, J.; Torres Cosme, R.; Rovira, J.; Ortiz, A.; Pascale, J.M.; Dimopoulos, G. Reciprocal Tripartite Interactions between the Aedes aegypti Midgut Microbiota, Innate Immune System and Dengue Virus Influences Vector Competence. PLoS Neglected Trop. Dis. 2012, 6, e1561. [Google Scholar] [CrossRef]
  235. Moreira, L.A.; Iturbe-Ormaetxe, I.; Jeffery, J.A.; Lu, G.; Pyke, A.T.; Hedges, L.M.; Rocha, B.C.; Hall-Mendelin, S.; Day, A.; Riegler, M. A Wolbachia Symbiont in Aedes aegypti Limits Infection with Dengue, Chikungunya, and Plasmodium. Cell 2009, 139, 1268–1278. [Google Scholar] [CrossRef]
  236. Walker, T.; Johnson, P.H.; Moreira, L.A.; Iturbe-Ormaetxe, I.; Frentiu, F.D.; McMeniman, C.J.; Leong, Y.S.; Dong, Y.; Axford, J.; Kriesner, P. The w Mel Wolbachia Strain Blocks Dengue and Invades Caged Aedes aegypti Populations. Nature 2011, 476, 450–453. [Google Scholar] [CrossRef]
  237. Aliota, M.T.; Peinado, S.A.; Velez, I.D.; Osorio, J.E. The WMel Strain of Wolbachia Reduces Transmission of Zika Virus by Aedes aegypti. Sci. Rep. 2016, 6, 28792. [Google Scholar] [CrossRef]
  238. Ryan, P.A.; Turley, A.P.; Wilson, G.; Hurst, T.P.; Retzki, K.; Brown-Kenyon, J.; Hodgson, L.; Kenny, N.; Cook, H.; Montgomery, B.L. Establishment of WMel Wolbachia in Aedes aegypti Mosquitoes and Reduction of Local Dengue Transmission in Cairns and Surrounding Locations in Northern Queensland, Australia. Gates Open Res. 2019, 3, 1547. [Google Scholar]
  239. Nazni, W.A.; Hoffmann, A.A.; NoorAfizah, A.; Cheong, Y.L.; Mancini, M.V.; Golding, N.; Kamarul, G.M.; Arif, M.A.; Thohir, H.; NurSyamimi, H. Establishment of Wolbachia Strain WAlbB in Malaysian Populations of Aedes aegypti for Dengue Control. Curr. Biol. 2019, 29, 4241–4248.e5. [Google Scholar] [CrossRef] [PubMed]
  240. Fraser, J.E.; O’Donnell, T.B.; Duyvestyn, J.M.; O’Neill, S.L.; Simmons, C.P.; Flores, H.A. Novel Phenotype of Wolbachia Strain w Pip in Aedes aegypti Challenges Assumptions on Mechanisms of Wolbachia-Mediated Dengue Virus Inhibition. PLoS Pathog. 2020, 16, e1008410. [Google Scholar] [CrossRef]
  241. Caragata, E.P.; Rancès, E.; Hedges, L.M.; Gofton, A.W.; Johnson, K.N.; O’Neill, S.L.; McGraw, E.A. Dietary Cholesterol Modulates Pathogen Blocking by Wolbachia. PLoS Pathog. 2013, 9, e1003459. [Google Scholar] [CrossRef]
  242. Geoghegan, V.; Stainton, K.; Rainey, S.M.; Ant, T.H.; Dowle, A.A.; Larson, T.; Hester, S.; Charles, P.D.; Thomas, B.; Sinkins, S.P. Perturbed Cholesterol and Vesicular Trafficking Associated with Dengue Blocking in Wolbachia-Infected Aedes aegypti Cells. Nat. Commun. 2017, 8, 526. [Google Scholar] [CrossRef] [PubMed]
  243. Kambris, Z.; Cook, P.E.; Phuc, H.K.; Sinkins, S.P. Immune Activation by Life-Shortening Wolbachia and Reduced Filarial Competence in Mosquitoes. Science 2009, 326, 134–136. [Google Scholar] [CrossRef] [PubMed]
  244. Rancès, E.; Ye, Y.H.; Woolfit, M.; McGraw, E.A.; O’Neill, S.L. The Relative Importance of Innate Immune Priming in Wolbachia-Mediated Dengue Interference. PLoS Pathog. 2012, 8, e1002548. [Google Scholar] [CrossRef] [PubMed]
  245. Utarini, A.; Indriani, C.; Ahmad, R.A.; Tantowijoyo, W.; Arguni, E.; Ansari, M.R.; Supriyati, E.; Wardana, D.S.; Meitika, Y.; Ernesia, I. Efficacy of Wolbachia-Infected Mosquito Deployments for the Control of Dengue. N. Engl. J. Med. 2021, 384, 2177–2186. [Google Scholar] [CrossRef]
  246. Pinto, S.B.; Riback, T.I.; Sylvestre, G.; Costa, G.; Peixoto, J.; Dias, F.B.; Tanamas, S.K.; Simmons, C.P.; Dufault, S.M.; Ryan, P.A. Effectiveness of Wolbachia-Infected Mosquito Deployments in Reducing the Incidence of Dengue and Other Aedes-Borne Diseases in Niterói, Brazil: A Quasi-Experimental Study. PLoS Neglected Trop. Dis. 2021, 15, e0009556. [Google Scholar] [CrossRef] [PubMed]
  247. Dodson, B.L.; Pujhari, S.; Brustolin, M.L.; Metz, H.C.; Rasgon, J.L. Variable Effects of Wolbachia on Alphavirus Infection in Aedes aegypti. bioRxiv 2023. [Google Scholar] [CrossRef]
  248. Loreto, E.L.S.; Wallau, G.L. Risks of Wolbachia Mosquito Control. Science 2016, 351, 1273. [Google Scholar] [CrossRef]
  249. Sanaei, E.; Charlat, S.; Engelstädter, J. Wolbachia Host Shifts: Routes, Mechanisms, Constraints and Evolutionary Consequences. Biol. Rev. 2021, 96, 433–453. [Google Scholar] [CrossRef]
  250. Edenborough, K.M.; Flores, H.A.; Simmons, C.P.; Fraser, J.E. Using Wolbachia to Eliminate Dengue: Will the Virus Fight Back? J. Virol. 2021, 95, e02203-20. [Google Scholar] [CrossRef]
  251. Thi Hue Kien, D.; Edenborough, K.M.; da Silva Goncalves, D.; Thuy Vi, T.; Casagrande, E.; Thi Le Duyen, H.; Thi Long, V.; Thi Dui, L.; Thi Tuyet Nhu, V.; Thi Giang, N. Genome Evolution of Dengue Virus Serotype 1 under Selection by Wolbachia pipientis in Aedes aegypti Mosquitoes. Virus Evol. 2023, 3, vead016. [Google Scholar] [CrossRef]
  252. Wilke, A.B.B.; Marrelli, M.T. Paratransgenesis: A Promising New Strategy for Mosquito Vector Control. Parasites Vectors 2015, 8, 342. [Google Scholar] [CrossRef] [PubMed]
  253. Wang, S.; Jacobs-Lorena, M. Paratransgenesis Applications: Fighting Malaria with Engineered Mosquito Symbiotic Bacteria. In Arthropod Vector: Controller of Disease Transmission, Volume 1; Elsevier: Amsterdam, The Netherlands, 2017; pp. 219–234. [Google Scholar]
  254. Ratcliffe, N.A.; Furtado Pacheco, J.P.; Dyson, P.; Castro, H.C.; Gonzalez, M.S.; Azambuja, P.; Mello, C.B. Overview of Paratransgenesis as a Strategy to Control Pathogen Transmission by Insect Vectors. Parasites Vectors 2022, 15, 112. [Google Scholar]
  255. Wang, S.; Jacobs-Lorena, M. Transgenesis and Paratransgenesis for the Control of Malaria. In Mosquito Gene Drives and the Malaria Eradication Agenda; Jenny Stanford Publishing, United Square: Singapore, 2023; pp. 21–37. [Google Scholar]
  256. Huang, W.; Wang, S.; Jacobs-Lorena, M. Use of Microbiota to Fight Mosquito-Borne Disease. Front. Genet. 2020, 11, 196. [Google Scholar] [CrossRef]
  257. Yoshida, S.; Ioka, D.; Matsuoka, H.; Endo, H.; Ishii, A. Bacteria Expressing Single-Chain Immunotoxin Inhibit Malaria Parasite Development in Mosquitoes. Mol. Biochem. Parasitol. 2001, 113, 89–96. [Google Scholar] [CrossRef]
  258. Wang, S.; Ghosh, A.K.; Bongio, N.; Stebbings, K.A.; Lampe, D.J.; Jacobs-Lorena, M. Fighting Malaria with Engineered Symbiotic Bacteria from Vector Mosquitoes. Proc. Natl. Acad. Sci. USA 2012, 109, 12734–12739. [Google Scholar] [CrossRef] [PubMed]
  259. Wang, S.; Dos-Santos, A.L.; Huang, W.; Liu, K.C.; Oshaghi, M.A.; Wei, G.; Agre, P.; Jacobs-Lorena, M. Driving Mosquito Refractoriness to Plasmodium falciparum with Engineered Symbiotic Bacteria. Science 2017, 357, 1399–1402. [Google Scholar] [CrossRef] [PubMed]
  260. Villegas, L.M.; Pimenta, P.F.P. Metagenomics, Paratransgenesis and the Anopheles Microbiome: A Portrait of the Geographical Distribution of the Anopheline Microbiota Based on a Meta-Analysis of Reported Taxa. Memórias Inst. Oswaldo Cruz 2014, 109, 672–684. [Google Scholar] [CrossRef]
  261. Bongio, N.J.; Lampe, D.J. Inhibition of Plasmodium berghei Development in Mosquitoes by Effector Proteins Secreted from Asaia sp. Bacteria Using a Novel Native Secretion Signal. PLoS ONE 2015, 10, e0143541. [Google Scholar] [CrossRef] [PubMed]
  262. Mancini, M.V.; Spaccapelo, R.; Damiani, C.; Accoti, A.; Tallarita, M.; Petraglia, E.; Rossi, P.; Cappelli, A.; Capone, A.; Peruzzi, G. Paratransgenesis to Control Malaria Vectors: A Semi-Field Pilot Study. Parasites Vectors 2016, 9, 140. [Google Scholar] [CrossRef]
  263. Raharimalala, F.N.; Boukraa, S.; Bawin, T.; Boyer, S.; Francis, F. Molecular Detection of Six (Endo-) Symbiotic Bacteria in Belgian Mosquitoes: First Step towards the Selection of Appropriate Paratransgenesis Candidates. Parasitol. Res. 2016, 115, 1391–1399. [Google Scholar] [CrossRef]
  264. Rocha, E.M.; Marinotti, O.; Serrão, D.M.; Correa, L.V.; de Katak, R.M.; de Oliveira, J.C.; Muniz, V.A.; de Oliveira, M.R.; do Nascimento Neto, J.F.; Pessoa, M.C.F. Culturable Bacteria Associated with Anopheles darlingi and Their Paratransgenesis Potential. Malar. J. 2021, 20, 40. [Google Scholar] [CrossRef]
  265. Carballar-Lejarazú, R.; Rodriguez, M.H.; de la Cruz Hernández-Hernández, F.; Ramos-Castaneda, J.; Possani, L.D.; Zurita-Ortega, M.; Reynaud-Garza, E.; Hernández-Rivas, R.; Loukeris, T.; Lycett, G. Recombinant Scorpine: A Multifunctional Antimicrobial Peptide with Activity against Different Pathogens. Cell. Mol. Life Sci. 2008, 65, 3081–3092. [Google Scholar] [CrossRef] [PubMed]
  266. Ward, T.W.; Jenkins, M.S.; Afanasiev, B.N.; Edwards, M.; Duda, B.A.; Suchman, E.; Jacobs-Lorena, M.; Beaty, B.J.; Carlson, J.O. Aedes aegypti Transducing Densovirus Pathogenesis and Expression in Aedes aegypti and Anopheles gambiae Larvae. Insect Mol. Biol. 2001, 10, 397–405. [Google Scholar] [CrossRef] [PubMed]
  267. Carlson, J.; Suchman, E.; Buchatsky, L. Densoviruses for Control and Genetic Manipulation of Mosquitoes. Adv. Virus Res. 2006, 68, 361–392. [Google Scholar] [PubMed]
  268. Ren, X.; Hoiczyk, E.; Rasgon, J.L. Viral Paratransgenesis in the Malaria Vector Anopheles gambiae. PLoS Pathog. 2008, 4, e1000135. [Google Scholar] [CrossRef] [PubMed]
  269. Johnson, R.M.; Rasgon, J.L. Densonucleosis Viruses (‘Densoviruses’) for Mosquito and Pathogen Control. Curr. Opin. Insect Sci. 2018, 28, 90–97. [Google Scholar] [CrossRef]
  270. Riehle, M.A.; Moreira, C.K.; Lampe, D.; Lauzon, C.; Jacobs-Lorena, M. Using Bacteria to Express and Display Anti-Plasmodium Molecules in the Mosquito Midgut. Int. J. Parasitol. 2007, 37, 595–603. [Google Scholar] [CrossRef]
  271. Favia, G.; Ricci, I.; Marzorati, M.; Negri, I.; Alma, A.; Sacchi, L.; Bandi, C.; Daffonchio, D. Bacteria of the Genus Asaia: A Potential Paratransgenic Weapon against Malaria. Transgenes. Manag. Vector Borne Dis. 2008, 627, 49–59. [Google Scholar]
  272. Dehghan, H.; Mosa-Kazemi, S.H.; Yakhchali, B.; Maleki-Ravasan, N.; Vatandoost, H.; Oshaghi, M.A. Evaluation of Anti-Malaria Potency of Wild and Genetically Modified Enterobacter Cloacae Expressing Effector Proteins in Anopheles stephensi. Parasites Vectors 2022, 15, 63. [Google Scholar] [CrossRef] [PubMed]
  273. Rasgon, J.L. Using Infections to Fight Infections: Paratransgenic Fungi Can Block Malaria Transmission in Mosquitoes. Future Microbiol. 2011, 6, 851–853. [Google Scholar] [CrossRef] [PubMed]
  274. Tzschaschel, B.D.; Guzmán, C.A.; Timmis, K.N.; Lorenzo, V.d. An Escherichia coli Hemolysin Transport System-Based Vector for the Export of Polypeptides: Export of Shiga-like Toxin IIeB Subunit by Salmonella typhimurium AroA. Nat. Biotechnol. 1996, 14, 765–769. [Google Scholar] [CrossRef] [PubMed]
  275. Commission Regulation (EU) 2022/1438 of 31 August 2022. Amending Annex II to Regulation (EC) No 1107/2009 of the European Parliament and of the Council as Regards Specific Criteria for the Approval of Active Substances That Are Microorganisms (Text with EEA Relevance). Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32022R1438 (accessed on 16 July 2023).
  276. Rezende-Teixeira, P.; Dusi, R.G.; Jimenez, P.C.; Espindola, L.S.; Costa-Lotufo, L.V. What Can We Learn from Commercial Insecticides? Efficacy, Toxicity, Environmental Impacts, and Future Developments. Environ. Pollut. 2022, 300, 118983. [Google Scholar] [PubMed]
  277. Whitford, F.; Pike, D.; Burroughs, F.; Hanger, G.; Johnson, B.; Brassard, D.; Blessing, A. The Pesticide Marketplace, Discovering and Developing New Products. PPP-71. 2006. Available online: chrome-extension://efaidnbmnnnibpcajpcglclefindmkaj/https://www.extension.purdue.edu/extmedia/ppp/ppp-71.pdf (accessed on 16 July 2023).
  278. Roadmappers, T.I. A Roadmap for the Development of Ivermectin as a Complementary Malaria Vector Control Tool. Am. J. Trop. Med. Hyg. 2020, 102, 3–24. [Google Scholar] [CrossRef] [PubMed]
  279. Koul, O. Biopesticides: Commercial Opportunities and Challenges. Dev. Commer. Biopestic. 2023, 1–23. [Google Scholar] [CrossRef]
  280. Deshayes, C.; Siegwart, M.; Pauron, D.; Froger, J.-A.; Lapied, B.; Apaire-Marchais, V. Microbial Pest Control Agents: Are They a Specific and Safe Tool for Insect Pest Management? Curr. Med. Chem. 2017, 24, 2959–2973. [Google Scholar] [CrossRef]
  281. Beech, C.; Rose, N.; Dass, B. Regulation of Transgenic Insects. In Transgenic Insects: Techniques and Applications; CABI GB: London, UK, 2022; pp. 493–517. [Google Scholar]
Insects 14 00718 g001
Figure 1. Microorganisms and their applications for controlling vector populations and disease transmission. Microorganisms are sources of molecules with insecticide (biopesticides) antipathogen (biopharmaceuticals) activities. Interactions of environmental and symbiotic fungi and bacteria with mosquitoes and their microbiota may affect mosquito and pathogen survival, having implications for vector control and disease transmission. Research that elucidates these interactions is crucial because it underpins the development of novel biotechnological products aimed at effective vector control and reducing disease transmission. Created with BioRender.com (accessed on 5 August 2023).
Figure 1. Microorganisms and their applications for controlling vector populations and disease transmission. Microorganisms are sources of molecules with insecticide (biopesticides) antipathogen (biopharmaceuticals) activities. Interactions of environmental and symbiotic fungi and bacteria with mosquitoes and their microbiota may affect mosquito and pathogen survival, having implications for vector control and disease transmission. Research that elucidates these interactions is crucial because it underpins the development of novel biotechnological products aimed at effective vector control and reducing disease transmission. Created with BioRender.com (accessed on 5 August 2023).
Insects 14 00718 g001
Insects 14 00718 g002
Figure 2. Biotechnological potential of mosquito symbiotic bacteria against infectious agents. (A), secretion of toxic substances that either kill or arrest the development and replication of viruses and parasites. (B), formation of physical barriers through large population accumulation or rearrangements of molecules secreted into the midgut lumen, preventing the passage of parasites to organs essential for their successful development. (C), activation of the mosquito immune system, which not only reduces the load of symbiotic bacteria but also leads to the elimination of invading parasites through the secretion of toxic molecules, preventing their propagation in the mosquito’s body. (D), competition with infectious agents for space and nutrients can have dire consequences for these pathogens as they must compete with a vastly larger population of symbiotic bacteria in the mosquito’s midgut lumen. This results in limited resources for the pathogens, ultimately leading to their decreased survival and replication within the mosquito. (E), paratransgenesis involves populating vector insects with genetically engineered symbiotic microorganisms that effectively hinder the development of parasites through synthesizing and secreting antipathogen molecules. This topic is further explored in topic 4.3 of this review. Created with BioRender.com (accessed on 5 August 2023).
Figure 2. Biotechnological potential of mosquito symbiotic bacteria against infectious agents. (A), secretion of toxic substances that either kill or arrest the development and replication of viruses and parasites. (B), formation of physical barriers through large population accumulation or rearrangements of molecules secreted into the midgut lumen, preventing the passage of parasites to organs essential for their successful development. (C), activation of the mosquito immune system, which not only reduces the load of symbiotic bacteria but also leads to the elimination of invading parasites through the secretion of toxic molecules, preventing their propagation in the mosquito’s body. (D), competition with infectious agents for space and nutrients can have dire consequences for these pathogens as they must compete with a vastly larger population of symbiotic bacteria in the mosquito’s midgut lumen. This results in limited resources for the pathogens, ultimately leading to their decreased survival and replication within the mosquito. (E), paratransgenesis involves populating vector insects with genetically engineered symbiotic microorganisms that effectively hinder the development of parasites through synthesizing and secreting antipathogen molecules. This topic is further explored in topic 4.3 of this review. Created with BioRender.com (accessed on 5 August 2023).
Insects 14 00718 g002
Insects 14 00718 g003
Figure 3. Strategies for dissemination of GM microorganisms in the wild and their continual circulation among mosquitoes. (A) Male and female mosquitoes are fed in the laboratory with a sucrose solution containing the GM microorganisms and then released into the wild to mate with other wild mosquitoes. The spread of GM microorganisms can also occur through the provision of sucrose baits in the field enriched with GM microorganisms. This enables the GM microorganisms to be transmitted forward, allowing them to spread throughout the wild mosquito population and aiding in reducing vector-borne disease transmission. (B) Release of GM microorganisms into natural larval breeding sites. The GM microorganisms are ingested by the larvae and remain associated with them until adulthood. If mosquitoes become infected with a parasite that is a target of the effector molecules produced by the GM microorganisms, these molecules will interfere with the development of the target pathogen, thereby preventing its transmission. (C) Persistence of GM microorganisms in mosquitoes for generations through vertical and horizontal transmission. Vertical transmission occurs from parents to offspring, while horizontal transmission takes place between mosquitoes during mating or sharing of breeding sites. The presence of GM microorganisms can continue to impact mosquito populations for an extended period. Created with BioRender.com (accessed on 5 August 2023).
Figure 3. Strategies for dissemination of GM microorganisms in the wild and their continual circulation among mosquitoes. (A) Male and female mosquitoes are fed in the laboratory with a sucrose solution containing the GM microorganisms and then released into the wild to mate with other wild mosquitoes. The spread of GM microorganisms can also occur through the provision of sucrose baits in the field enriched with GM microorganisms. This enables the GM microorganisms to be transmitted forward, allowing them to spread throughout the wild mosquito population and aiding in reducing vector-borne disease transmission. (B) Release of GM microorganisms into natural larval breeding sites. The GM microorganisms are ingested by the larvae and remain associated with them until adulthood. If mosquitoes become infected with a parasite that is a target of the effector molecules produced by the GM microorganisms, these molecules will interfere with the development of the target pathogen, thereby preventing its transmission. (C) Persistence of GM microorganisms in mosquitoes for generations through vertical and horizontal transmission. Vertical transmission occurs from parents to offspring, while horizontal transmission takes place between mosquitoes during mating or sharing of breeding sites. The presence of GM microorganisms can continue to impact mosquito populations for an extended period. Created with BioRender.com (accessed on 5 August 2023).
Insects 14 00718 g003
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Katak, R.d.M.; Cintra, A.M.; Burini, B.C.; Marinotti, O.; Souza-Neto, J.A.; Rocha, E.M. Biotechnological Potential of Microorganisms for Mosquito Population Control and Reduction in Vector Competence. Insects 2023, 14, 718. https://doi.org/10.3390/insects14090718

AMA Style

Katak RdM, Cintra AM, Burini BC, Marinotti O, Souza-Neto JA, Rocha EM. Biotechnological Potential of Microorganisms for Mosquito Population Control and Reduction in Vector Competence. Insects. 2023; 14(9):718. https://doi.org/10.3390/insects14090718

Chicago/Turabian Style

Katak, Ricardo de Melo, Amanda Montezano Cintra, Bianca Correa Burini, Osvaldo Marinotti, Jayme A. Souza-Neto, and Elerson Matos Rocha. 2023. "Biotechnological Potential of Microorganisms for Mosquito Population Control and Reduction in Vector Competence" Insects 14, no. 9: 718. https://doi.org/10.3390/insects14090718

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop