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Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis

BACKGROUND: Insect microbiota is a dynamic microbial community that can actively participate in defense against pathogens. Bacillus thuringiensis (Bt) is a natural entomopathogen widely used as a bioinsecticide for pest control. Although Bt’s mode of action has been extensively studied, whether the...

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Autores principales: Tetreau, Guillaume, Grizard, Stéphanie, Patil, Chandrashekhar D., Tran, Florence-Hélène, Tran Van, Van, Stalinski, Renaud, Laporte, Frédéric, Mavingui, Patrick, Després, Laurence, Valiente Moro, Claire
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834902/
https://www.ncbi.nlm.nih.gov/pubmed/29499735
http://dx.doi.org/10.1186/s13071-018-2741-8
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author Tetreau, Guillaume
Grizard, Stéphanie
Patil, Chandrashekhar D.
Tran, Florence-Hélène
Tran Van, Van
Stalinski, Renaud
Laporte, Frédéric
Mavingui, Patrick
Després, Laurence
Valiente Moro, Claire
author_facet Tetreau, Guillaume
Grizard, Stéphanie
Patil, Chandrashekhar D.
Tran, Florence-Hélène
Tran Van, Van
Stalinski, Renaud
Laporte, Frédéric
Mavingui, Patrick
Després, Laurence
Valiente Moro, Claire
author_sort Tetreau, Guillaume
collection PubMed
description BACKGROUND: Insect microbiota is a dynamic microbial community that can actively participate in defense against pathogens. Bacillus thuringiensis (Bt) is a natural entomopathogen widely used as a bioinsecticide for pest control. Although Bt’s mode of action has been extensively studied, whether the presence of microbiota is mandatory for Bt to effectively kill the insect is still under debate. An association between a higher tolerance and a modified microbiota was already evidenced but a critical point remained to be solved: is the modified microbiota a cause or a consequence of a higher tolerance to Bt? METHODS: In this study we focused on the mosquito species Aedes aegypti, as no work has been performed on Diptera on this topic to date, and on B. thuringiensis israelensis (Bti), which is used worldwide for mosquito control. To avoid using antibiotics to cure bacterial microbiota, mosquito larvae were exposed to an hourly increasing dose of Bti during 25 hours to separate the most susceptible larvae dying quickly from more tolerant individuals, with longer survival. RESULTS: Denaturing gradient gel electrophoresis (DGGE) fingerprinting revealed that mosquito larval bacterial microbiota was strongly affected by Bti infection after only a few hours of exposure. Bacterial microbiota from the most tolerant larvae showed the lowest diversity but the highest inter-individual differences. The proportion of Bti in the host tissue was reduced in the most tolerant larvae as compared to the most susceptible ones, suggesting an active control of Bti infection by the host. CONCLUSIONS: Here we show that a modified microbiota is associated with a higher tolerance of mosquitoes to Bti, but that it is rather a consequence of Bti infection than the cause of the higher tolerance. This study paves the way to future investigations aiming at unraveling the role of host immunity, inter-species bacterial competition and kinetics of host colonization by Bti that could be at the basis of the phenotype observed in this study. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-018-2741-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-58349022018-03-05 Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis Tetreau, Guillaume Grizard, Stéphanie Patil, Chandrashekhar D. Tran, Florence-Hélène Tran Van, Van Stalinski, Renaud Laporte, Frédéric Mavingui, Patrick Després, Laurence Valiente Moro, Claire Parasit Vectors Research BACKGROUND: Insect microbiota is a dynamic microbial community that can actively participate in defense against pathogens. Bacillus thuringiensis (Bt) is a natural entomopathogen widely used as a bioinsecticide for pest control. Although Bt’s mode of action has been extensively studied, whether the presence of microbiota is mandatory for Bt to effectively kill the insect is still under debate. An association between a higher tolerance and a modified microbiota was already evidenced but a critical point remained to be solved: is the modified microbiota a cause or a consequence of a higher tolerance to Bt? METHODS: In this study we focused on the mosquito species Aedes aegypti, as no work has been performed on Diptera on this topic to date, and on B. thuringiensis israelensis (Bti), which is used worldwide for mosquito control. To avoid using antibiotics to cure bacterial microbiota, mosquito larvae were exposed to an hourly increasing dose of Bti during 25 hours to separate the most susceptible larvae dying quickly from more tolerant individuals, with longer survival. RESULTS: Denaturing gradient gel electrophoresis (DGGE) fingerprinting revealed that mosquito larval bacterial microbiota was strongly affected by Bti infection after only a few hours of exposure. Bacterial microbiota from the most tolerant larvae showed the lowest diversity but the highest inter-individual differences. The proportion of Bti in the host tissue was reduced in the most tolerant larvae as compared to the most susceptible ones, suggesting an active control of Bti infection by the host. CONCLUSIONS: Here we show that a modified microbiota is associated with a higher tolerance of mosquitoes to Bti, but that it is rather a consequence of Bti infection than the cause of the higher tolerance. This study paves the way to future investigations aiming at unraveling the role of host immunity, inter-species bacterial competition and kinetics of host colonization by Bti that could be at the basis of the phenotype observed in this study. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13071-018-2741-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-03-02 /pmc/articles/PMC5834902/ /pubmed/29499735 http://dx.doi.org/10.1186/s13071-018-2741-8 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Tetreau, Guillaume
Grizard, Stéphanie
Patil, Chandrashekhar D.
Tran, Florence-Hélène
Tran Van, Van
Stalinski, Renaud
Laporte, Frédéric
Mavingui, Patrick
Després, Laurence
Valiente Moro, Claire
Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis
title Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis
title_full Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis
title_fullStr Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis
title_full_unstemmed Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis
title_short Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis
title_sort bacterial microbiota of aedes aegypti mosquito larvae is altered by intoxication with bacillus thuringiensis israelensis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5834902/
https://www.ncbi.nlm.nih.gov/pubmed/29499735
http://dx.doi.org/10.1186/s13071-018-2741-8
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