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Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception

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A special issue of Pathogens (ISSN 2076-0817).

Deadline for manuscript submissions: closed (31 August 2023) | Viewed by 11877

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Special Issue Editor

Dr. Francesca Scolari

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Guest Editor

Institute of Molecular Genetics, National Research Council (IGM-CNR), Pavia, Italy
Interests: Francesca’s research is mainly focused on unravelling the genomic, molecular and physiological bases of the reproductive biology of insect agricultural pests and disease vectors

Special Issue Information

Dear Colleagues,

Insect pathogens can manipulate the interactions occurring between disease vectors and vertebrate hosts as well as between agricultural pests and plant hosts. Effects of pathogens on the biology of vectors and on their behavior have been described in several systems, including those related to public health diseases such as malaria, sleeping sickness, and leishmaniasis. These manipulations may promote pathogen transmission, although contrasting findings have been reported, further pointing at the complexity of insect–pathogen interplay. Plant viruses transmitted by insects can manipulate vector behavior and host plant physiology, revealing a network of interactions coordinated through environmental dynamics.

Malaria parasites influence the physiology of mosquitoes, affecting feeding behavior and host-seeking through alterations in olfactory sensitivity. Arboviruses, including Zika and Dengue viruses, have been shown to mediate behavioral changes in mosquito hosts affecting not only host-seeking but also oviposition preferences. However, the underlying mechanisms remain to be clarified, similarly to the interactions taking place between direct pathogen-mediated effects and general immune responses. Likewise, the behavior of insect vectors of plant pathogens is affected by both the pathogen effects on plant cues mediating infected/healthy host plant discrimination and the direct effects of the pathogen on the physiology of insect vectors, including cue perception.

Insects integrate a wide set of sensory cues to locate their hosts. These include not only olfactory but also thermal and visual stimuli. Understanding the features of the tripartite systems involving insect, pathogen, and host to determine their effects on insect sensory perception has wide implications not only to expand knowledge on human and plant diseases’ transmission, but also to develop targeted insect control strategies.

The aim of this Special Issue is to highlight recent findings on the effects of insect–pathogen (e.g., viruses, bacteria, protozoa, fungi) interplay on insect sensory perception, also to pave the way for innovative sustainable pest and disease management strategies.

In this Special Issue, we invite you to contribute with studies centered on different aspects of the relationships between insects and pathogens affecting insect sensory perception. Topics of interest include but are not limited to the description of i) the pathogen-mediated effects on insect sensory behavior, pathogen transmission, and host fitness, ii) the physiological and molecular mechanisms underlying these effects, and iii) the impact of both the ecological context and insect microbiota in shaping pathogen-mediated effects on host physiology.

Both original research and review articles are welcome.

We look forward to your contribution.

Dr. Francesca Scolari
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Pathogens is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2700 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

behavioral changes
olfactory sensitivity
pathogen transmission
insect vectors
agricultural pests

Published Papers (7 papers)

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Research

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18 pages, 2047 KiB

Open AccessArticle

Influence of RVFV Infection on Olfactory Perception and Behavior in Drosophila melanogaster

by Stella Bergmann, Maja C. Bohn, Susann Dornbusch, Stefanie C. Becker and Michael Stern

Pathogens 2023, 12(4), 558; https://doi.org/10.3390/pathogens12040558 - 05 Apr 2023

Cited by 2 | Viewed by 1576

Abstract

In blood-feeding dipterans, olfaction plays a role in finding hosts and, hence, in spreading pathogens. Several pathogens are known to alter olfactory responses and behavior in vectors. As a mosquito-borne pathogen, Rift Valley Fever Virus (RVFV) can affect humans and cause great losses in livestock. We test the influence of RVFV infection on sensory perception, olfactory choice behavior and activity on a non-biting insect, Drosophila melanogaster, using electroantennograms (EAG), Y-maze, and locomotor activity monitor. Flies were injected with RVFV MP12 strain. Replication of RVFV and its persistence for at least seven days was confirmed by quantitative reverse transcription-PCR (RT-qPCR). One day post injection, infected flies showed weaker EAG responses towards 1-hexanol, vinegar, and ethyl acetate. In the Y-maze, infected flies showed a significantly lower response for 1-hexanol compared to uninfected flies. At days six or seven post infection, no significant difference between infected and control flies could be found in EAG or Y-maze anymore. Activity of infected flies was reduced at both time points. We found an upregulation of the immune-response gene, nitric oxide synthase, in infected flies. An infection with RVFV is able to transiently reduce olfactory perception and attraction towards food-related odors in Drosophila, while effects on activity and immune effector gene expression persist. A similar effect in blood-feeding insects could affect vector competence in RVFV transmitting dipterans. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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21 pages, 12843 KiB

Open AccessArticle

Antimicrobial Potential of Betulinic Acid and Investigation of the Mechanism of Action against Nuclear and Metabolic Enzymes with Molecular Modeling

by Gabriela Cristina Soares Rodrigues, Mayara dos Santos Maia, Thalisson Amorim de Souza, Edeltrudes de Oliveira Lima, Luiz Eduardo Carneiro Gomes dos Santos, Shellygton Lima Silva, Marcelo Sobral da Silva, José Maria Barbosa Filho, Valnês da Silva Rodrigues Junior, Luciana Scotti and Marcus Tullius Scotti

Pathogens 2023, 12(3), 449; https://doi.org/10.3390/pathogens12030449 - 13 Mar 2023

Cited by 4 | Viewed by 1576

Abstract

Natural products have important pharmacological activities. This study sought to investigate the activity of the compound betulinic acid (BA) against different strains of bacteria and fungi. The minimum inhibitory concentration (MIC) was determined and then the minimum bactericidal concentration (MBC) and minimum fungicidal concentration (MFC). After performing the in vitro tests, molecular modeling studies were carried out to investigate the mechanism of action of BA against the selected microorganisms. The results showed that BA inhibited the growth of microbial species. Among the 12 species (Staphylococcus aureus, S. epidermidis, Pseudomonas aeruginosa, Escherichia coli, Mycobacterium tuberculosis, Candida albicans, C. tropicalis, C. glabrata, Aspergillus flavus, Penicillium citrinum, Trichophyton rubrum, and Microsporum canis) investigated, 9 (75%) inhibited growth at a concentration of 561 µM and 1 at a concentration of 100 µM. In general, the MBC and MFC of the products were between 561 and 1122 μM. In silico studies showed that BA presented a mechanism of action against DNA gyrase and beta-lactamase targets for most of the bacteria investigated, while for fungi the mechanism of action was against sterol 14α-demethylase (CYP51) targets and dihydrofolate reductase (DHFR). We suggest that BA has antimicrobial activity against several species. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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12 pages, 2371 KiB

Open AccessArticle

The Phytopathogen Fusarium verticillioides Modifies the Intestinal Morphology of the Sugarcane Borer

by Diego Z. Gallan, Maressa O. Henrique and Marcio C. Silva-Filho

Pathogens 2023, 12(3), 443; https://doi.org/10.3390/pathogens12030443 - 11 Mar 2023

Cited by 1 | Viewed by 1284

Abstract

Background: In tropical sugarcane crops, the fungus Fusarium verticillioides, the agent responsible for the occurrence of the red rot complex, occurs in association with the sugarcane borer Diatraea saccharalis. This fungus, in addition to being transmitted vertically, can manipulate both the insect and the plant for its own dissemination in the field. Due to the complex interaction between F. verticillioides and D. saccharalis, and the high incidence of the fungus in the intestinal region, our objective was to investigate whether F. verticillioides could alter the intestinal structure of the insect. Methods: We combined analysis of scanning electron microscopy and light microscopy to identify whether the presence of the fungus F. verticillioides, in artificial diets or in sugarcane, could lead to any alteration or regional preference in the insect’s intestinal ultrastructure over the course of its development, or its offspring development, analyzing the wall and microvillous structures of the mid-digestive system. Results: Here, we show that the fungus F. verticillioides alters the intestinal morphology of D. saccharalis, promoting an increase of up to 3.3 times in the thickness of the midgut compared to the control. We also observed that the phytopathogen colonizes the intestinal microvilli for reproduction, suggesting that this region can be considered the gateway of the fungus to the insect’s reproductive organs. In addition, the colonization of this region promoted the elongation of microvillous structures by up to 180% compared to the control, leading to an increase in the area used for colonization. We also used the fungus Colletotrichum falcatum in the tests, and it did not differ from the control in any test, showing that this interaction is specific between D. saccharalis and F. verticillioides. Conclusions: The phytopathogenic host F. verticillioides alters the intestinal morphology of the vector insect in favor of its colonization. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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13 pages, 4178 KiB

Open AccessArticle

Chalcone Derivative Induces Flagellar Disruption and Autophagic Phenotype in Phytomonas serpens In Vitro

by Tamiris A. C. Santos, Kleiton P. Silva, Gabriella B. Souza, Péricles B. Alves, Rubem F. S. Menna-Barreto, Ricardo Scher and Roberta P. M. Fernandes

Pathogens 2023, 12(3), 423; https://doi.org/10.3390/pathogens12030423 - 07 Mar 2023

Cited by 1 | Viewed by 1153

Abstract

Phytomonas serpens is a trypanosomatid phytoparasite, found in a great variety of species, including tomato plants. It is a significant problem for agriculture, causing high economic loss. In order to reduce the vegetal infections, different strategies have been used. The biological activity of molecules obtained from natural sources has been widely investigated to treat trypanosomatids infections. Among these compounds, chalcones have been shown to have anti-parasitic and anti-inflammatory effects, being described as having a remarkable activity on trypanosomatids, especially in Leishmania species. Here, we evaluated the antiprotozoal activity of the chalcone derivative (NaF) on P. serpens promastigotes, while also assessing its mechanism of action. The results showed that treatment with the derivative NaF for 24 h promotes an important reduction in the parasite proliferation (IC₅₀/24 h = 23.6 ± 4.6 µM). At IC₅₀/24 h concentration, the compound induced an increase in reactive oxygen species (ROS) production and a shortening of the unique flagellum of the parasites. Electron microscopy evaluation reinforced the flagellar phenotype in treated promastigotes, and a dilated flagellar pocket was frequently observed. The treatment also promoted a prominent autophagic phenotype. An increased number of autophagosomes were detected, presenting different levels of cargo degradation, endoplasmic reticulum profiles surrounding different cellular structures, and the presence of concentric membranar structures inside the mitochondrion. Chalcone derivatives may present an opportunity to develop a treatment for the P. serpens infection, as they are easy to synthesize and are low in cost. In order to develop a new product, further studies are still necessary. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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10 pages, 860 KiB

Open AccessArticle

Secretion and Detection of Defensive Compounds by the Red Flour Beetle Tribolium castaneum Interacting with the Insect Pathogenic Fungus Beauveria bassiana

by Belén Davyt-Colo, Juan R. Girotti, Andrés González and Nicolás Pedrini

Pathogens 2022, 11(5), 487; https://doi.org/10.3390/pathogens11050487 - 20 Apr 2022

Cited by 4 | Viewed by 1885

Abstract

Entomopathogenic fungi such as Beauveria bassiana are extensively used for the control of insect pests worldwide. They infect mostly by adhesion to the insect surface and penetration through the cuticle. However, some insects, such as the red flour beetle Tribolium castaneum (Herbst), have evolved resistance by embedding their cuticle with antifungal compounds. Thus, they avoid fungal germination on the cuticle, which result in low susceptibility to entomopathogenic fungi. In adult T. castaneum, these antifungals are the well-known defensive compounds methyl-1,4- and ethyl-1,4-benzoquinone. In this study, we added B. bassiana conidia on the diet of adult beetles to study the effect of the entomopathogen on the secretion and detection of the beetle volatile blend containing both benzoquinones. The compounds were analyzed by solid phase microextraction coupled to gas chromatography–flame ionization detection, and were detected by electroantennography. In addition, we measured the expression level of four genes encoding for two odorant-binding proteins (OBP), one chemosensory protein (CSP), and one odorant receptor (OR) in both healthy and fungus-treated insects. Significant alterations in the secretion of both benzoquinones, as well as in the perception of methyl-1,4-benzoquinone, were found in fungus-treated insects. TcOBP7D, TcOBP0A and TcCSP3A genes were down-regulated in insects fed conidia for 12 and 48 h, and the latter gene was up-regulated in 72 h samples. TcOR1 expression was not altered at the feeding times studied. We conclude that fungus-treated insects alter both secretion and perception of benzoquinones, but additional functional and genetic studies are needed to fully understand the effects of fungal infection on the insect chemical ecology. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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Review

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22 pages, 878 KiB

Open AccessReview

Pathogen-Mediated Alterations of Insect Chemical Communication: From Pheromones to Behavior

by Andrea Moyano, Anna Cleta Croce and Francesca Scolari

Pathogens 2023, 12(11), 1350; https://doi.org/10.3390/pathogens12111350 - 14 Nov 2023

Viewed by 1213

Abstract

Pathogens can influence the physiology and behavior of both animal and plant hosts in a manner that promotes their own transmission and dispersal. Recent research focusing on insects has revealed that these manipulations can extend to the production of pheromones, which are pivotal in chemical communication. This review provides an overview of the current state of research and available data concerning the impacts of bacterial, viral, fungal, and eukaryotic pathogens on chemical communication across different insect orders. While our understanding of the influence of pathogenic bacteria on host chemical profiles is still limited, viral infections have been shown to induce behavioral changes in the host, such as altered pheromone production, olfaction, and locomotion. Entomopathogenic fungi affect host chemical communication by manipulating cuticular hydrocarbons and pheromone production, while various eukaryotic parasites have been observed to influence insect behavior by affecting the production of pheromones and other chemical cues. The effects induced by these infections are explored in the context of the evolutionary advantages they confer to the pathogen. The molecular mechanisms governing the observed pathogen-mediated behavioral changes, as well as the dynamic and mutually influential relationships between the pathogen and its host, are still poorly understood. A deeper comprehension of these mechanisms will prove invaluable in identifying novel targets in the perspective of practical applications aimed at controlling detrimental insect species. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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11 pages, 1103 KiB

Open AccessEditor’s ChoiceReview

The Role of Parasitoid Wasps, Ixodiphagus spp. (Hymenoptera: Encyrtidae), in Tick Control

by Rafael Antonio Nascimento Ramos, Lucia Oliveira de Macedo, Marcos Antônio Bezerra-Santos, Gílcia Aparecida de Carvalho, Guilherme Gomes Verocai and Domenico Otranto

Pathogens 2023, 12(5), 676; https://doi.org/10.3390/pathogens12050676 - 03 May 2023

Cited by 3 | Viewed by 1948

Abstract

Species of Ixodiphagus (Hymenoptera: Encyrtidae) are parasitoid wasps whose immature forms develop inside ixodid and argasid ticks (Acari: Ixodida). Following oviposition by adult female wasps into the idiosoma of ticks, larvae hatch and start feeding on their internal contents, eventually emerging as adult wasps from the body of the dead ticks. Species of Ixodiphagus have been reported as parasitoids of 21 species of ticks distributed across 7 genera. There are at least ten species described in the genus, with Ixodiphagus hookeri being the most studied as an agent for biological control of ticks. Although attempts of tick control by means of this parasitoid largely failed, in a small-scale study 150,000 specimens of I. hookeri were released over a 1-year period in a pasture where a small cattle population was kept, resulting in an overall reduction in the number of Amblyomma variegatum ticks per animal. This review discusses current scientific information about Ixodiphagus spp., focusing on the role of this parasitoid in the control of ticks. The interactions between these wasps and the ticks’ population are also discussed, focusing on the many biological and logistical challenges, with limitations of this control method for reducing tick populations under natural conditions. Full article

(This article belongs to the Special Issue Insect-Pathogen Dynamic Interplay and its Effects on Sensory-Perception)

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