Potential for Bacillus thuringiensis and Other Bacterial Toxins as Biological Control Agents to Combat Dipteran Pests of Medical and Agronomic Importance
Abstract
:1. Introduction
2. The Entomopathogenic Bacterium Bacillus thuringiensis
3. Importance of Dipteran Control
4. Dipteran-Active Insecticidal Bacterial Toxins
4.1. Bt Toxins Active against Diptera
Family | Name (Former Name) | Insect Target | Activity Range LC50 (µg/mL) | References | |
---|---|---|---|---|---|
Family | Species | ||||
Cry1 | Cry1Ab7 | Culicidae | Aedes aegypti | ND a | [34] |
Cry1Ac8 | Glossinidae | Glossina morsitans | 0.42–0.74 a | [35] | |
Cry1Ba1 | Muscidae | Musca domestica | 20 a | [36] | |
Calliphoridae | Lucilia cuprina | ND a,b | [37,38] | ||
Cry1Bc1 | Muscidae | Musca domestica | 79.4 a | [37] | |
Calliphoridae | Lucilia cuprina | 308 a | [37] | ||
Chrysomya albiceps | 807 a | [37] | |||
Cry1Ca1 | Culicidae | Aedes aegypti | 39.3–141 a | [39,40] | |
Anopheles gambiae | 143–283 a | [39] | |||
Culex quinquefasciatus | 126 a | [39] | |||
Cry2 | Cry2Aa1 | Culicidae | Aedes aegypti | 37.06–79.46 a,b | [41,42,43,44] |
Anopheles quadrimaculatus | 0.37 a | [44] | |||
Aedes triseriatus (Ochlerotatus triseriatus) | 2.84 a | [44] | |||
Culex quinquefasciatus | 0.53 a | [45] | |||
Cry2Aa2 | Culicidae | Culex quinquefasciatus | 1.63 a | [46] | |
Cry2Aa4 | Culicidae | Aedes aegypti | ND a | [47] | |
Anopheles stephensi | ND a | [47] | |||
Culex quinquefasciatus (Culex fatigans) | ND a | [47] | |||
Cry2Aa14 | Culicidae | Culex quinquefasciatus | 0.894 a | [48] | |
Cry2Aa | Culicidae | Anopheles gambiae | 0.11 a | [49] | |
Cry2Ab1 | Culicidae | Aedes aegypti | 23.42–35.80 a,b | [6,43,50,51,52] | |
Cry2Ab2 | Culicidae | Anopheles gambiae | 0.54 a | [49] | |
Cry2Ab25 | Tephritidae | Rhagoletis cerasi | ND b | [53] | |
Cry2Ac11 | Culicidae | Aedes aegypti | [6] | ||
Cry2Ag | Culicidae | Aedes aegypti | 2.54 b | [51] | |
Cry2Am1 | Culicidae | Aedes aegypti | [6] | ||
Cry4 | Cry4Aa1 | Culicidae | Aedes aegypti | 0.03–13 a,b | [54,55,56,57,58,59,60,61,62,63] |
Anopheles gambiae | 1.07–1.17 a | [55] | |||
Anopheles stephensi | 0.52–7.4 a,b | [59,60,61,64] | |||
Culex pipiens | 0.25–0.97 a | [54,59,60,61,65] | |||
Culex quinquefasciatus | 0.05–5.04 a,b | [33,54,55,66] | |||
Simuliidae | Simulium spp. | ND b | [67] | ||
Cry4Ba1 | Chironomidae | Chironomus tepperi | 0.94 b | [68] | |
Culicidae | Aedes aegypti | 0.12–0.94 a,b | [54,55,57,58,59,61,64,69] | ||
Anopheles albimanus | 1.3 b | [70] | |||
Anopheles gambiae | 0.79 a | [55] | |||
Anopheles quadrimaculatus | 0.25 a | [54] | |||
Anopheles stephensi | 0.55–17 a,b | [59,61,64] | |||
Culex quinquefasciatus | 24.5 a | [55] | |||
Culicidae | Culex pipiens | ND b | [64] | ||
Tipulidae | Tipula oleracea | ND a | [71] | ||
Simuliidae | Simulium spp. | ND b | [67] | ||
Cry4Ba2 | Culicidae | Aedes aegypti | ND a | [72] | |
Cry4Cb1 | Culicidae | Aedes aegypti | 0.083 b | [73] | |
Cry10 | Cry10Aa | Culicidae | Aedes aegypti | 0.3–20.61 a,b | [62,74] |
Cry11 | Cry11Aa1 | Chironomidae | Chironomus tepperi | 0.56 b | [68] |
Culicidae | Aedes aegypti | 0.01-1.35 a,b | [41,42,57,58,61,75,76,77,78,79] | ||
Anopheles albimanus | 0.9 b | [70] | |||
Anopheles stephensi | 0.13-0.45 a,b | [60,75,78,80,81] | |||
Anopheles albimanus | 6.759 a | [77] | |||
Culex pipiens | 0.009-0.27 a | [75,78] | |||
Culex quinquefasciatus | 0.01-0.13 a,b | [45,66,76,77,82,83] | |||
Tipulidae | Tipula oleracea | ND b | [81] | ||
Simuliidae | Simulium spp. | ND b | [67] | ||
Cry11Ba1 | Culicidae | Aedes aegypti | 0.02–0.03 a,b | [75,77,84] | |
Anopheles albimanus | 0.10 a | [77] | |||
Anopheles stephensi | 0.04 a | [75] | |||
Culex pipiens | 0.01–0.11 a | [61,65] | |||
Culex quinquefasciatus | 0.006–0.02 a,b | [77,83,84] | |||
Cry11Bb1 | Culicidae | Aedes aegypti | 0.02–0.85 a,b | [76,77,85,86] | |
Anopheles albimanus | 0.17 a | [77] | |||
Anopheles stephensi | 0.07 a | [85] | |||
Culex pipiens | 0.04 a | [85] | |||
Culex quinquefasciatus | 0.01–0.13 a,b | [76,77,86] | |||
Cry16-Cry17-Cbm17.1-Cbm17.2 | Cry16-Cry17-Cbm17.1-Cbm17.2 | Culicidae | Aedes aegypti | ND b | [87] |
Cry19 | Cry19Aa | Culicidae | Anopheles stephensi | 1.04 a | [88] |
Culex pipiens | 0.19 a | [88] | |||
Cry19B | Culicidae | Culex pipiens molestus | 5.93 a | [89] | |
Cry20 | Cry20Aa1 | Culicidae | Aedes aegypti | 648 b | [90] |
Culex quinquefasciatus | 700 b | [90] | |||
Cry24 | Cry24Ca1 | Culicidae | Aedes aegypti | 0.48 b | [91] |
Cry27 | Cry27Aa1 | Culicidae | Anopheles stephensi | 94.3 a | [92] |
Cry30 | Cry30Fa1 | Culicidae | Aedes aegypti | 15.4 a | [93] |
Cry30Ga1 | Culicidae | Aedes aegypti | 7.10 b | [73] | |
Cry39 | Cry39Aa1 | Culicidae | Anopheles stephensi | 0.75 b | [94] |
Culex pipiens | 41.94 b | [95] | |||
Cry44 | Cry44Aa1 | Culicidae | Aedes aegypti | 0.01 a | [60] |
Anopheles stephensi | 1.26 a | [60] | |||
Culex pipiens | 0.006 a | [60] | |||
Mpp46 | Mpp46Ab (Cry46Ab) | Culicidae | Culex pipiens | 1.02 a | [96] |
Cry47 | Cry47Aa1 | Calliphoridae | Lucilia cuprina | ND a | [97,98] |
Cry50 | Cry50Ba | Culicidae | Culex quinquefasciatus | 0.07 a | [99] |
Cry54 | Cry54Aa1 | Culicidae | Aedes aegypti | 9.02 a | [100] |
Cry56 | Cry56Aa1 | Culicidae | Aedes aegypti | 0.15 a | [101] |
Mpp60 | Mpp60Aa (Cry60Aa) | Culicidae | Culex quinquefasciatus | 7.9 b | [102] |
Mpp60Ba (Cry60Ba) | Culicidae | Culex quinquefasciatus | 5.5 b | [102] | |
Mpp60Aa+Mpp60Ba (Cry60Aa+Cry60Ba) | Culicidae | Culex quinquefasciatus | 2.9 b | [102] | |
Tpp80 | Tpp80Aa1 (Cry80Aa1) | Culicidae | Culex pipiens pallens | 71.9 a | [103] |
Cyt1 | Cyt1Aa1 | Calliphoridae | Calliphora stygia | 305 a | [104] |
Lucilia cuprina | 296 a | [104] | |||
Lucilia sericata | 236 a | [104] | |||
Chironomidae | Chironomus tepperi | 31 b | [68] | ||
Culicidae | Aedes aegypti | 0.15–1.86 a,b | [74,105,106,107,108,109] | ||
Anopheles stephensi | 2.7–6.3 a | [105,108] | |||
Culex pipiens | 0.6–1.2 a | [105,108] | |||
Culex quinquefasciatus | 0.4 a | [108] | |||
Tephritidae | Ceratitis capitata | ND a | [26] | ||
Tipulidae | Tipula paludosa | ND a | [110] | ||
Cyt1Aa2 | Culicidae | Aedes aegypti | 0.12–1.21 a,b | [58,63,111] | |
Anopheles gambiae | 1–2 a,b | [111] | |||
Culex pipiens | 0.5–2 a,b | [111] | |||
Cyt1Aa4 | Culicidae | Aedes aegypti | 0.06 a | [79] | |
Culex quinquefasciatus | >10 a | [112] | |||
Cyt1Ab1 | Culicidae | Aedes aegypti | 32.6–59 a,b | [105,113] | |
Anopheles stephensi | 20 a | [105] | |||
Culex pipiens | 5.7 a | [105] | |||
Culex quinquefasciatus | 32.9–114.5 b | [113] | |||
Cyt1Ba1 | Agromyzidae | Liriomyza trifolii | ND a | [114] | |
Cyt2 | Cyt2Aa1 | Culicidae | Aedes aegypti | 1–4 a,b | [111] |
Anopheles gambiae | 1–2 a,b | [111] | |||
Culex pipiens | 0.5–4 a,b | [111] | |||
Cyt2Aa2 | Culicidae | Aedes aegypti | 0.35–0.5 a | [69,115] | |
Culex quinquefasciatus | 0.25–0.5 a | [69,115] | |||
Cyt2Aa3 | Chironomidae | Chironomus tepperi | 36 a | [116] | |
Culicidae | Culex quinquefasciatus | 0.53 a | [116] | ||
Cyt2Ba1 | Culicidae | Aedes aegypti | 0.28–33 a,b | [62,108,113,117] | |
Anopheles stephensi | 5.5 a | [108] | |||
Culex pipiens | 5 a | [108] | |||
Culex quinquefasciatus | 1.8–31.5 a,b | [108,113] | |||
Cyt2Bb1 | Culicidae | Aedes aegypti | 6.8 b | [106] | |
Cyt2Bc1 | Culicidae | Aedes aegypti | 7 a | [108] | |
Anopheles stephensi | 11 a | [108] | |||
Culex pipiens | 7.3 a | [108] | |||
Culex quinquefasciatus | 1.8 a | [108] | |||
Mtx | Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 0.01 a | [118] |
Aedes aegypti | 0.05 a | [118] | |||
Chironomidae | Chironomus riparius | 4.06 a | [119] | ||
Mpp2 | Mpp2Aa1 (Mtx2) | Culicidae | Culex quinquefasciatus | 4.13–107 b | [66] |
Mpp2Aa1 (Mtx2 strain SSII-1) | Culicidae | Culex quinquefasciatus | 0.93 a | [120] | |
Aedes aegypti | 14.5 a | [120] | |||
Mpp2Aa2 Mtx2 (31-2) | Culicidae | Culex quinquefasciatus | 3.90 a | [120] | |
Aedes aegypti | 3.91 a | [120] | |||
Mpp3 | Mpp3Aa1 (Mtx3) | Culicidae | Culex quinquefasciatus | ND a | [121] |
Aedes aegypti | ND a | [121] | |||
Monalysin | Monalysin | Drosophilidae | Drosophila melanogaster | ND a | [122] |
CpbA | CpbA | Muscidae | Musca domestica | ND a | [123] |
CpbB | CpbB | Muscidae | Musca domestica | ND a | [123] |
CHRD | CHRD | Muscidae | Musca domestica | ND a | [123] |
ExsC | ExsC | Muscidae | Musca domestica | ND a | [123] |
Pmp1 | Pmp1 | Culicidae | Anopheles coluzzii | ND a | [124] |
Two part toxins | Cry48Aa/Tpp49 (Cry49Aa) | Culicidae | Culex quinquefasciatus | 0.02/0.006 a | [125] |
Tpp1/Tpp2 (BinA/BinB) | Culicidae | Aedes aegypti | 42 a | [126,127] | |
Aedes atropalpus | ND a | [126] | |||
Anopheles gambiae | 0.36 a | [127] | |||
Anopheles stephensi | 0.39 a | [127] | |||
Anopheles albimanus | 1 a | [127] | |||
Anopheles quadrimaculatus | 4.6 a | [127] | |||
Culex pipiens | 0.1 a | [127] | |||
Culicidae | Culex quinquefasciatus | 0.013–0.03 a,b | [126,128] | ||
Pra/Prb (PirA/PirB) | Culicidae | Aedes aegypti | ND a | [84,129] | |
Synergy | Cry1Ca/Cyt1Aa | Culicidae | Aedes aegypti | 0.61 a | [130] |
Cry2Aa/Cry2Ab | Culicidae | Aedes aegypti | 51.3 b | [43] | |
Cry2Aa/Cry50Ba | Culicidae | Culex quinquefasciatus | 0.05 a | [99] | |
Cry4Aa/Cry4Ba | Culicidae | Aedes aegypti | 0.05 a | [61] | |
Anopheles stephensi | 0.02 a | [61] | |||
Culex pipiens | 0.04 a | [61] | |||
Culex quinquefasciatus | 1.49–315 b | [66] | |||
Simuliidae | Simulium spp. | ND b | [67] | ||
Cry4Aa/Cyt1Aa | Culicidae | Aedes aegypti | 0.07 a | [58] | |
Chironomidae | Chironomus tepperi | 44 b | [68] | ||
Tipulidae | Tipula paludosa | ND a | [110] | ||
Cry4Aa/Cyt2Ba | Culicidae | Aedes aegypti | 0.013 b | [62,131] | |
Cry4Aa/Cry11Ba | Culicidae | Culex pipiens | 0.04 a | [65] | |
Cry4Aa/Cry46Ab | Culicidae | Culex pipiens | 0.18 a | [96] | |
Cry4A/Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 1.06–2.37 b | [66] | |
Cry4A/Mpp2Aa1 (Mtx2) | Culicidae | Culex quinquefasciatus | 0.27–1.21 b | [66] | |
Cry4Ba/Cry11Aa | Culicidae | Anopheles albimanus | 0.567 b | [70] | |
Simuliidae | Simulium spp. | ND b | [67] | ||
Cry4Ba/Cyt1Aa | Culicidae | Aedes aegypti | 0.62 a | [58] | |
Culicidae | Anopheles albimanus | 0.33–0.77 b | [70] | ||
Cry4Ba/Cyt2Aa2 | Culicidae | Aedes aegypti | 0.007 a | [69] | |
Culex quinquefasciatus | 0.02 a | [69] | |||
Cry4B/Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 18.2–29.0 b | [66] | |
Cry4B/Mpp2Aa1 (Mtx2) | Culicidae | Culex quinquefasciatus | 85.7 b | [66] | |
Cry10Aa/Cyt1Aa | Culicidae | Aedes aegypti | 0.03–0.08 a,b | [74] | |
Cry10Aa/Cyt2Ba | Culicidae | Aedes aegypti | 0.004 b | [62] | |
Cry11Aa/Cyt1Aa | Culicidae | Aedes aegypti | 0.01–0.12 a | [58,79] | |
Culicidae | Anopheles albimanus | 0.28–0.37 b | [70] | ||
Cry11/Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 0.66–3.03 b | [66] | |
Cry11/Mpp2Aa1 (Mtx2) | Culex quinquefasciatus | 0.90 b | [66] | ||
Cry11Bb/Cry29Aa | Culicidae | Aedes aegypti | 3.94 a | [85] | |
Anopheles stephensi | 2.13 a | [85] | |||
Culex pipiens | 0.73 a | [85] | |||
Cry11Bb/Cry30Aa | Culicidae | Aedes aegypti | 16.96 a | [85] | |
Anopheles stephensi | 1.43 a | [85] | |||
Culex pipiens | 1.13 a | [85] | |||
Cry4A/Cry4B/Cry11A | Culicidae | Aedes aegypti | 0.12 a | [58] | |
Culex quinquefasciatus | 0.008–0.59 b | [66] | |||
Cry4A/Cry4B/Cyt1A | Culicidae | Aedes aegypti | 0.08 a | [58] | |
Cry4A/Cry4B/Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 0.18–0.77 b | [66] | |
Cry4A/Cry4B/Mpp2Aa1 (Mtx2) | Culicidae | Culex quinquefasciatus | 0.11–0.32 b | [66] | |
Cry4A/Cry4B/Cry11A/Cyt1A | Culicidae | Aedes aegypti | 0.08 a | [58] | |
Culex quinquefasciatus | 0.02–0.07 b | [66] | |||
Cry4A/Cry4B/Cry11A/Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 0.02–0.24 b | [66] | |
Cry4A/Cry4B/Cry11A/Mpp2Aa1 (Mtx2) | Culicidae | Culex quinquefasciatus | 0.03–0.06 b | [66] | |
Cry4A/Cry4B/Cry11A/Cyt1A/Mtx1Aa1 | Culicidae | Culex quinquefasciatus | 0.02–0.06 b | [66] | |
Cry4A/Cry4B/Cry11A/Cyt1A/Mpp2Aa1(Mtx2) | Culicidae | Culex quinquefasciatus | 0.30–1.09 b | [66] | |
Cry4Ba/Cry11Aa/Cyt1Aa | Culicidae | Anopheles albimanus | 0.7–8.33 b | [70] | |
Cry11Bb/Cry29Aa/Cry30Aa | Culicidae | Aedes aegypti | 5.43 a | [85] | |
Anopheles stephensi | 1.31 a | [85] | |||
Culex pipiens | 0.85 a | [85] |
4.1.1. Cry Toxins from Bt ser. israelensis
Cry4 Proteins
Cry10Aa Protein
Cry11 Proteins
Mpp60A/Mpp60B Proteins (Formerly Cry60A/Cry60B)
4.1.2. Other Toxins Specific to Diptera
4.1.3. Anti-Dipteran Toxins with Cross-Order Activity
Cry1 Protein
Cry2A Protein
Other Cry Proteins
4.1.4. Anti-Dipteran Cyt Toxins
Cyt1 Proteins
Cyt2 Proteins
4.2. Anti-Dipteran Toxins from Other Microorganisms
4.2.1. Toxins from Lysinibacillus sphaericus
4.2.2. Toxins from Paraclostridium bifermentans
4.2.3. Other Dipteran-Active Proteins
5. Toxins with Synergistic Activity against Diptera
6. Bacterial Insecticides against Mosquitoes
7. Concluding Remarks and Future Perspectives
Funding
Conflicts of Interest
References
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Valtierra-de-Luis, D.; Villanueva, M.; Berry, C.; Caballero, P. Potential for Bacillus thuringiensis and Other Bacterial Toxins as Biological Control Agents to Combat Dipteran Pests of Medical and Agronomic Importance. Toxins 2020, 12, 773. https://doi.org/10.3390/toxins12120773
Valtierra-de-Luis D, Villanueva M, Berry C, Caballero P. Potential for Bacillus thuringiensis and Other Bacterial Toxins as Biological Control Agents to Combat Dipteran Pests of Medical and Agronomic Importance. Toxins. 2020; 12(12):773. https://doi.org/10.3390/toxins12120773
Chicago/Turabian StyleValtierra-de-Luis, Daniel, Maite Villanueva, Colin Berry, and Primitivo Caballero. 2020. "Potential for Bacillus thuringiensis and Other Bacterial Toxins as Biological Control Agents to Combat Dipteran Pests of Medical and Agronomic Importance" Toxins 12, no. 12: 773. https://doi.org/10.3390/toxins12120773
APA StyleValtierra-de-Luis, D., Villanueva, M., Berry, C., & Caballero, P. (2020). Potential for Bacillus thuringiensis and Other Bacterial Toxins as Biological Control Agents to Combat Dipteran Pests of Medical and Agronomic Importance. Toxins, 12(12), 773. https://doi.org/10.3390/toxins12120773