The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>

ABSTRACT Endosymbiotic Wolbachia bacteria and the gut microbiome have independently been shown to affect several aspects of insect biology, including reproduction, development, life span, stem cell activity, and resistance to human pathogens, in insect vectors. This work shows that Wolbachia bacteri...

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Autores principales:	Rama K. Simhadri, Eva M. Fast, Rong Guo, Michaela J. Schultz, Natalie Vaisman, Luis Ortiz, Joanna Bybee, Barton E. Slatko, Horacio M. Frydman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Drosophila microbiome gut microbiome symbiosis Wolbachia Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e5a766ae78bf4e3db960a9172d154811
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spelling	oai:doaj.org-article:e5a766ae78bf4e3db960a9172d1548112021-11-15T15:22:05ZThe Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>10.1128/mSphere.00287-172379-5042https://doaj.org/article/e5a766ae78bf4e3db960a9172d1548112017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00287-17https://doaj.org/toc/2379-5042ABSTRACT Endosymbiotic Wolbachia bacteria and the gut microbiome have independently been shown to affect several aspects of insect biology, including reproduction, development, life span, stem cell activity, and resistance to human pathogens, in insect vectors. This work shows that Wolbachia bacteria, which reside mainly in the fly germline, affect the microbial species present in the fly gut in a lab-reared strain. Drosophila melanogaster hosts two main genera of commensal bacteria—Acetobacter and Lactobacillus. Wolbachia-infected flies have significantly reduced titers of Acetobacter. Sampling of the microbiome of axenic flies fed with equal proportions of both bacteria shows that the presence of Wolbachia bacteria is a significant determinant of the composition of the microbiome throughout fly development. However, this effect is host genotype dependent. To investigate the mechanism of microbiome modulation, the effect of Wolbachia bacteria on Imd and reactive oxygen species pathways, the main regulators of immune response in the fly gut, was measured. The presence of Wolbachia bacteria does not induce significant changes in the expression of the genes for the effector molecules in either pathway. Furthermore, microbiome modulation is not due to direct interaction between Wolbachia bacteria and gut microbes. Confocal analysis shows that Wolbachia bacteria are absent from the gut lumen. These results indicate that the mechanistic basis of the modulation of composition of the microbiome by Wolbachia bacteria is more complex than a direct bacterial interaction or the effect of Wolbachia bacteria on fly immunity. The findings reported here highlight the importance of considering the composition of the gut microbiome and host genetic background during Wolbachia-induced phenotypic studies and when formulating microbe-based disease vector control strategies. IMPORTANCE Wolbachia bacteria are intracellular bacteria present in the microbiome of a large fraction of insects and parasitic nematodes. They can block mosquitos’ ability to transmit several infectious disease-causing pathogens, including Zika, dengue, chikungunya, and West Nile viruses and malaria parasites. Certain extracellular bacteria present in the gut lumen of these insects can also block pathogen transmission. However, our understanding of interactions between Wolbachia and gut bacteria and how they influence each other is limited. Here we show that the presence of Wolbachia strain wMel changes the composition of gut commensal bacteria in the fruit fly. Our findings implicate interactions between bacterial species as a key factor in determining the overall composition of the microbiome and thus reveal new paradigms to consider in the development of disease control strategies.Rama K. SimhadriEva M. FastRong GuoMichaela J. SchultzNatalie VaismanLuis OrtizJoanna BybeeBarton E. SlatkoHoracio M. FrydmanAmerican Society for MicrobiologyarticleDrosophila microbiomegut microbiomesymbiosisWolbachiaMicrobiologyQR1-502ENmSphere, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Drosophila microbiome gut microbiome symbiosis Wolbachia Microbiology QR1-502
spellingShingle	Drosophila microbiome gut microbiome symbiosis Wolbachia Microbiology QR1-502 Rama K. Simhadri Eva M. Fast Rong Guo Michaela J. Schultz Natalie Vaisman Luis Ortiz Joanna Bybee Barton E. Slatko Horacio M. Frydman The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>
description	ABSTRACT Endosymbiotic Wolbachia bacteria and the gut microbiome have independently been shown to affect several aspects of insect biology, including reproduction, development, life span, stem cell activity, and resistance to human pathogens, in insect vectors. This work shows that Wolbachia bacteria, which reside mainly in the fly germline, affect the microbial species present in the fly gut in a lab-reared strain. Drosophila melanogaster hosts two main genera of commensal bacteria—Acetobacter and Lactobacillus. Wolbachia-infected flies have significantly reduced titers of Acetobacter. Sampling of the microbiome of axenic flies fed with equal proportions of both bacteria shows that the presence of Wolbachia bacteria is a significant determinant of the composition of the microbiome throughout fly development. However, this effect is host genotype dependent. To investigate the mechanism of microbiome modulation, the effect of Wolbachia bacteria on Imd and reactive oxygen species pathways, the main regulators of immune response in the fly gut, was measured. The presence of Wolbachia bacteria does not induce significant changes in the expression of the genes for the effector molecules in either pathway. Furthermore, microbiome modulation is not due to direct interaction between Wolbachia bacteria and gut microbes. Confocal analysis shows that Wolbachia bacteria are absent from the gut lumen. These results indicate that the mechanistic basis of the modulation of composition of the microbiome by Wolbachia bacteria is more complex than a direct bacterial interaction or the effect of Wolbachia bacteria on fly immunity. The findings reported here highlight the importance of considering the composition of the gut microbiome and host genetic background during Wolbachia-induced phenotypic studies and when formulating microbe-based disease vector control strategies. IMPORTANCE Wolbachia bacteria are intracellular bacteria present in the microbiome of a large fraction of insects and parasitic nematodes. They can block mosquitos’ ability to transmit several infectious disease-causing pathogens, including Zika, dengue, chikungunya, and West Nile viruses and malaria parasites. Certain extracellular bacteria present in the gut lumen of these insects can also block pathogen transmission. However, our understanding of interactions between Wolbachia and gut bacteria and how they influence each other is limited. Here we show that the presence of Wolbachia strain wMel changes the composition of gut commensal bacteria in the fruit fly. Our findings implicate interactions between bacterial species as a key factor in determining the overall composition of the microbiome and thus reveal new paradigms to consider in the development of disease control strategies.
format	article
author	Rama K. Simhadri Eva M. Fast Rong Guo Michaela J. Schultz Natalie Vaisman Luis Ortiz Joanna Bybee Barton E. Slatko Horacio M. Frydman
author_facet	Rama K. Simhadri Eva M. Fast Rong Guo Michaela J. Schultz Natalie Vaisman Luis Ortiz Joanna Bybee Barton E. Slatko Horacio M. Frydman
author_sort	Rama K. Simhadri
title	The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>
title_short	The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>
title_full	The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>
title_fullStr	The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>
title_full_unstemmed	The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>
title_sort	gut commensal microbiome of <named-content content-type="genus-species">drosophila melanogaster</named-content> is modified by the endosymbiont <italic toggle="yes">wolbachia</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/e5a766ae78bf4e3db960a9172d154811
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The Gut Commensal Microbiome of <named-content content-type="genus-species">Drosophila melanogaster</named-content> Is Modified by the Endosymbiont <italic toggle="yes">Wolbachia</italic>

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