Persistence ofBacillus thuringiensis israelensis(Bti) in the environment induces resistance to multipleBtitoxins in mosquitoes

Paris, Margot; Tetreau, Guillaume; Laurent, Fabien; Lélu, Maud; Després, Laurence; David, Jean‐Philippe

doi:10.1002/ps.2046

Cited by 101 publications

(100 citation statements)

References 72 publications

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“…israelensis can recycle and achieve a high level of toxicity for mosquito larvae. Considering that mosquitoes can become resistant when selected with these toxic leaf litters in the laboratory (31,41), it can be expected that mosquito larvae exposed to field-persistent B. thuringiensis subsp. israelensis in some breeding sites may already be developing resistance to at least some toxins (Fig.…”

Section: Discussionmentioning

confidence: 99%

Fate of Bacillus thuringiensis subsp. israelensis in the Field: Evidence for Spore Recycling and Differential Persistence of Toxins in Leaf Litter

Tetreau

Alessi

Veyrenc

et al. 2012

Appl Environ Microbiol

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Bacillus thuringiensis subsp. israelensis is a bioinsecticide increasingly used worldwide for mosquito control. Despite its apparent low level of persistence in the field due to the rapid loss of its insecticidal activity, an increasing number of studies suggested that the recycling of B. thuringiensis subsp. israelensis can occur under specific, unknown conditions. Decaying leaf litters sampled in mosquito breeding sites in the French Rhône-Alpes region several months after a treatment were shown to exhibit a high level of larval toxicity and contained large amounts of spores. In the present article, we show that the high concentration of toxins found in these litters is consistent with spore recycling in the field, which gave rise to the production of new crystal toxins. Furthermore, in these toxic leaf litter samples, Cry4Aa and Cry4Ba toxins became the major toxins instead of Cyt1Aa in the commercial mixture. In a microcosm experiment performed in the laboratory, we also demonstrated that the toxins, when added in their crystal form to nontoxic leaf litter, exhibited patterns of differential persistence consistent with the proportions of toxins observed in the field-collected toxic leaf litter samples (Cry4 > Cry11 > Cyt). These results give strong evidence that B. thuringiensis subsp. israelensis recycled in specific breeding sites containing leaf litters, and one would be justified in asking whether mosquitoes can become resistant when exposed to field-persistent B. thuringiensis subsp. israelensis for several generations.

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Section: Discussionmentioning

confidence: 99%

Fate of Bacillus thuringiensis subsp. israelensis in the Field: Evidence for Spore Recycling and Differential Persistence of Toxins in Leaf Litter

Tetreau

Alessi

Veyrenc

et al. 2012

Appl Environ Microbiol

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“…However, the observation that Bti toxic crystals may persist in the environment has raised some concern that intensive applications could lead to accumulation of toxins with adverse effect on non‐target organisms (Boisvert & Boisvert, 1999; Dupont & Boisvert, 1986; Paris et al., 2011; Tilquin et al., 2008). An extensive review of the effect Bti on target and non‐target organisms has listed a number of studies indicating some negative effects on non‐target organisms (Boisvert & Boisvert, 2000).…”

Section: Introductionmentioning

confidence: 99%

Microbial larvicides for mosquito control: Impact of long lasting formulations ofBacillus thuringiensisvar.israelensisandBacillus sphaericuson non‐target organisms in western Kenya highlands

Derua

Kahindi

Mosha

et al. 2018

Ecology and Evolution

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The microbial larvicides Bacillus thuringiensis var. israelensis and Bacillus sphaericus have been used extensively for mosquito control and have been found to be effective and safe to non‐target organisms cohabiting with mosquito larvae. Recently developed long lasting microbial larvicides (LLML), although evading the previous challenge of short duration of activity, increase the risk of persistence of toxins in the treated larval habitats. This study monitored the impact of LLML FourStar® and LL3 on non‐target organisms cohabiting with mosquito larvae in an operational study to control malaria vectors in western Kenya highlands. A total of 300 larval habitats were selected in three highland villages. The habitats were first monitored for 5 weeks to collect baseline data on non‐target organisms cohabiting with mosquito larvae and then randomized into two treatment arms (respective FourStar® and LL3) and one control arm. Non‐target organisms were sampled weekly for 5 months after treatment to assess the impact of LLML intervention. Before treatment, the mean density of all non‐target organisms combined in the control, LL3 and FourStar® treated habitats was 1.42, 1.39 and 1.49 individuals per habitat per sampling occasion, respectively. Following treatment, this density remained fairly unchanged for 21 weeks at which time it was 1.82, 2.11, and 2.05 for the respective control, LL3 and FourStar® treated habitats. Statistical analysis revealed that LL3 and FourStar® did not significantly alter abundance, richness or diversity of the 11 taxa studied, when comparing the intervention and control larval habitats. However, both FourStar® and LL3 significantly reduced the density of malaria vectors. In conclusion, one round of label rate application of FourStar® or LL3 in natural larval habitats did not alter richness, abundance or diversity of the monitored aquatic non‐target organisms cohabiting with mosquito larvae to an ecologically significant level.

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“…These strains were obtained from the Pasteur Institute (Paris, France) or from B. Federici (University of California, Riverside). Spores and crystal suspensions were produced as previously described (29) and conserved in water at Ϫ20°C until use. Toxins were quantified on SDS-PAGE using bovine serum albumin (BSA) as a standard.…”

Section: Methodsmentioning

confidence: 99%

“…To test for the effect of the insecticide formulation, we also tested a nonformulated B. thuringiensis subsp. israelensis strain produced in the laboratory using spores isolated from VectoBac (1.7 ng/ml) as previously described (29). Larval mortality was monitored after 24 h. The effect of treatment (contaminated versus noncontaminated) on larval mortality was tested by a linear model performed with R 2.8.1 software (33).…”

Section: 500 International Toxic Units [Itu] · Mgmentioning

confidence: 99%

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Decreased Toxicity of Bacillus thuringiensis subsp. israelensis to Mosquito Larvae after Contact with Leaf Litter

Tetreau

Stalinski

Kersusan

et al. 2012

Appl Environ Microbiol

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Bacillus thuringiensis subsp. israelensis is a bacterium producing crystals containing Cry and Cyt proteins, which are toxic for mosquito larvae. Nothing is known about the interaction between crystal toxins and decaying leaf litter, which is a major component of several mosquito breeding sites and represents an important food source. In the present work, we investigated the behavior of B. thuringiensis subsp. israelensis toxic crystals sprayed on leaf litter. In the presence of leaf litter, a 60% decrease in the amount of Cyt toxin detectable by immunology (enzyme-linked immunosorbent assays [ELISAs]) was observed, while the respective proportions of Cry toxins were not affected. The toxicity of Cry toxins toward Aedes aegypti larvae was not affected by leaf litter, while the synergistic effect of Cyt toxins on all B. thuringiensis subsp. israelensis Cry toxins was decreased by about 20% when mixed with leaf litter. The toxicity of two commercial B. thuringiensis subsp. israelensis strains (VectoBac WG and VectoBac 12AS) and a laboratory-produced B. thuringiensis subsp. israelensis strain decreased by about 70% when mixed with leaf litter. Taken together, these results suggest that Cyt toxins interact with leaf litter, resulting in a decreased toxicity of B. thuringiensis subsp. israelensis in litter-rich environments and thereby dramatically reducing the efficiency of mosquitocidal treatments.

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Persistence ofBacillus thuringiensis israelensis(Bti) in the environment induces resistance to multipleBtitoxins in mosquitoes

Abstract: Considering that resistance to Cry toxins might act as a first step to resistance to a complete Bti toxin mixture, the present results highlight the importance of testing each toxin individually in order accurately to monitor Bti toxin resistance evolution in field populations.

Cited by 101 publications

References 72 publications

Fate of Bacillus thuringiensis subsp. israelensis in the Field: Evidence for Spore Recycling and Differential Persistence of Toxins in Leaf Litter

Fate of Bacillus thuringiensis subsp. israelensis in the Field: Evidence for Spore Recycling and Differential Persistence of Toxins in Leaf Litter

Microbial larvicides for mosquito control: Impact of long lasting formulations ofBacillus thuringiensisvar.israelensisandBacillus sphaericuson non‐target organisms in western Kenya highlands

Decreased Toxicity of Bacillus thuringiensis subsp. israelensis to Mosquito Larvae after Contact with Leaf Litter

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