The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>

ABSTRACT The vector-borne disease leishmaniasis, caused by Leishmania species protozoa, is transmitted to humans by phlebotomine sand flies. Development of Leishmania to infective metacyclic promastigotes in the insect gut, a process termed metacyclogenesis, is an essential prerequisite for transmis...

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Autores principales:	Patrick H. Kelly, Sarah M. Bahr, Tiago D. Serafim, Nadim J. Ajami, Joseph F. Petrosino, Claudio Meneses, John R. Kirby, Jesus G. Valenzuela, Shaden Kamhawi, Mary E. Wilson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d6dd89872da046f8a1e1c0dc1b822334
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spelling	oai:doaj.org-article:d6dd89872da046f8a1e1c0dc1b8223342021-11-15T15:51:07ZThe Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>10.1128/mBio.01121-162150-7511https://doaj.org/article/d6dd89872da046f8a1e1c0dc1b8223342017-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01121-16https://doaj.org/toc/2150-7511ABSTRACT The vector-borne disease leishmaniasis, caused by Leishmania species protozoa, is transmitted to humans by phlebotomine sand flies. Development of Leishmania to infective metacyclic promastigotes in the insect gut, a process termed metacyclogenesis, is an essential prerequisite for transmission. Based on the hypothesis that vector gut microbiota influence the development of virulent parasites, we sequenced midgut microbiomes in the sand fly Lutzomyia longipalpis with or without Leishmania infantum infection. Sucrose-fed sand flies contained a highly diverse, stable midgut microbiome. Blood feeding caused a decrease in microbial richness that eventually recovered. However, bacterial richness progressively decreased in L. infantum-infected sand flies. Acetobacteraceae spp. became dominant and numbers of Pseudomonadaceae spp. diminished coordinately as the parasite underwent metacyclogenesis and parasite numbers increased. Importantly, antibiotic-mediated perturbation of the midgut microbiome rendered sand flies unable to support parasite growth and metacyclogenesis. Together, these data suggest that the sand fly midgut microbiome is a critical factor for Leishmania growth and differentiation to its infective state prior to disease transmission. IMPORTANCE Leishmania infantum, a parasitic protozoan causing fatal visceral leishmaniasis, is transmitted to humans through the bite of the sand fly Lutzomyia longipalpis. Development of the parasite to its virulent metacyclic state occurs in the sand fly gut. In this study, the microbiota within the Lu. longipalpis midgut was delineated by 16S ribosomal DNA (rDNA) sequencing, revealing a highly diverse community composition that lost diversity as parasites developed to their metacyclic state and increased in abundance in infected flies. Perturbing sand fly gut microbiota with an antibiotic cocktail, which alone had no effect on either the parasite or the fly, arrested both the development of virulent parasites and parasite expansion. These findings indicate the importance of bacterial commensals within the insect vector for the development of virulent pathogens, and raise the possibility that impairing the microbial composition within the vector might represent a novel approach to control of vector-borne diseases.Patrick H. KellySarah M. BahrTiago D. SerafimNadim J. AjamiJoseph F. PetrosinoClaudio MenesesJohn R. KirbyJesus G. ValenzuelaShaden KamhawiMary E. WilsonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 1 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Patrick H. Kelly Sarah M. Bahr Tiago D. Serafim Nadim J. Ajami Joseph F. Petrosino Claudio Meneses John R. Kirby Jesus G. Valenzuela Shaden Kamhawi Mary E. Wilson The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>
description	ABSTRACT The vector-borne disease leishmaniasis, caused by Leishmania species protozoa, is transmitted to humans by phlebotomine sand flies. Development of Leishmania to infective metacyclic promastigotes in the insect gut, a process termed metacyclogenesis, is an essential prerequisite for transmission. Based on the hypothesis that vector gut microbiota influence the development of virulent parasites, we sequenced midgut microbiomes in the sand fly Lutzomyia longipalpis with or without Leishmania infantum infection. Sucrose-fed sand flies contained a highly diverse, stable midgut microbiome. Blood feeding caused a decrease in microbial richness that eventually recovered. However, bacterial richness progressively decreased in L. infantum-infected sand flies. Acetobacteraceae spp. became dominant and numbers of Pseudomonadaceae spp. diminished coordinately as the parasite underwent metacyclogenesis and parasite numbers increased. Importantly, antibiotic-mediated perturbation of the midgut microbiome rendered sand flies unable to support parasite growth and metacyclogenesis. Together, these data suggest that the sand fly midgut microbiome is a critical factor for Leishmania growth and differentiation to its infective state prior to disease transmission. IMPORTANCE Leishmania infantum, a parasitic protozoan causing fatal visceral leishmaniasis, is transmitted to humans through the bite of the sand fly Lutzomyia longipalpis. Development of the parasite to its virulent metacyclic state occurs in the sand fly gut. In this study, the microbiota within the Lu. longipalpis midgut was delineated by 16S ribosomal DNA (rDNA) sequencing, revealing a highly diverse community composition that lost diversity as parasites developed to their metacyclic state and increased in abundance in infected flies. Perturbing sand fly gut microbiota with an antibiotic cocktail, which alone had no effect on either the parasite or the fly, arrested both the development of virulent parasites and parasite expansion. These findings indicate the importance of bacterial commensals within the insect vector for the development of virulent pathogens, and raise the possibility that impairing the microbial composition within the vector might represent a novel approach to control of vector-borne diseases.
format	article
author	Patrick H. Kelly Sarah M. Bahr Tiago D. Serafim Nadim J. Ajami Joseph F. Petrosino Claudio Meneses John R. Kirby Jesus G. Valenzuela Shaden Kamhawi Mary E. Wilson
author_facet	Patrick H. Kelly Sarah M. Bahr Tiago D. Serafim Nadim J. Ajami Joseph F. Petrosino Claudio Meneses John R. Kirby Jesus G. Valenzuela Shaden Kamhawi Mary E. Wilson
author_sort	Patrick H. Kelly
title	The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>
title_short	The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>
title_full	The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>
title_fullStr	The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>
title_full_unstemmed	The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>
title_sort	gut microbiome of the vector <italic toggle="yes">lutzomyia longipalpis</italic> is essential for survival of <italic toggle="yes">leishmania infantum</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/d6dd89872da046f8a1e1c0dc1b822334
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The Gut Microbiome of the Vector <italic toggle="yes">Lutzomyia longipalpis</italic> Is Essential for Survival of <italic toggle="yes">Leishmania infantum</italic>

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