The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

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

doi:10.1128/mBio.01121-16

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The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

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The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

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 and Mary E Wilson

mBio, Vol.8(1), p.e01121-16

01/17/2017

DOI: 10.1128/mBio.01121-16

PMCID: PMC5241394

PMID: 28096483

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https://doi.org/10.1128/mBio.01121-16View

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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. 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.

Animals

Psychodidae - microbiology

Cell Survival

Gastrointestinal Microbiome

Bacteria - classification

RNA, Ribosomal, 16S - genetics

Disease Vectors

Bacteria - genetics

DNA, Ribosomal - chemistry

Sequence Analysis, DNA

Leishmania infantum - physiology

DNA, Ribosomal - genetics

Details

Title: Subtitle: The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum
Creators: Patrick H Kelly - Departments of Microbiology, Internal Medicine and Epidemiology, University of Iowa, Iowa City, Iowa, USA
Sarah M Bahr - Departments of Microbiology, Internal Medicine and Epidemiology, University of Iowa, Iowa City, Iowa, USA
Tiago D Serafim - Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, USA
Nadim J Ajami - Department of Molecular Virology and Microbiology, Alkek Center for Metagenomics and Microbiome Research, Baylor College of Medicine, Houston, Texas, USA
Joseph F Petrosino - Department of Molecular Virology and Microbiology, Alkek Center for Metagenomics and Microbiome Research, Baylor College of Medicine, Houston, Texas, USA
Claudio Meneses - Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, USA
John R Kirby - Departments of Microbiology, Internal Medicine and Epidemiology, University of Iowa, Iowa City, Iowa, USA
Jesus G Valenzuela - Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, USA
Shaden Kamhawi - Vector Molecular Biology Section, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, Maryland, USA
Mary E Wilson - Iowa City Veterans' Affairs Medical Center, Iowa City, Iowa, USA
Resource Type: Journal article
Publication Details: mBio, Vol.8(1), p.e01121-16
DOI: 10.1128/mBio.01121-16
PMID: 28096483
PMCID: PMC5241394
NLM abbreviation: mBio
ISSN: 2161-2129
eISSN: 2150-7511
Publisher: United States
Grant note: P50 AI074321 / NIAID NIH HHS T32 AI007511 / NIAID NIH HHS R01 AI076233 / NIAID NIH HHS P50 AI030639 / NIAID NIH HHS
Language: English
Date published: 01/17/2017
Academic Unit: Microbiology and Immunology; International Programs; Epidemiology; Internal Medicine
Record Identifier: 9984001132802771

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