Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya

The mosquito gut represents an ecosystem that accommodates a complex, intimately associated microbiome. It is increasingly clear that the gut microbiome influences a wide variety of host traits, such as fitness and immunity. Understanding the microbial community structure and its dynamics across mos...

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Veröffentlicht in:PloS one 2011-09, Vol.6 (9), p.e24767-e24767
Hauptverfasser: Wang, Ying, Gilbreath, 3rd, Thomas M, Kukutla, Phanidhar, Yan, Guiyun, Xu, Jiannong
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Gilbreath, 3rd, Thomas M
Kukutla, Phanidhar
Yan, Guiyun
Xu, Jiannong
description The mosquito gut represents an ecosystem that accommodates a complex, intimately associated microbiome. It is increasingly clear that the gut microbiome influences a wide variety of host traits, such as fitness and immunity. Understanding the microbial community structure and its dynamics across mosquito life is a prerequisite for comprehending the symbiotic relationship between the mosquito and its gut microbial residents. Here we characterized gut bacterial communities across larvae, pupae and adults of Anopheles gambiae reared in semi-natural habitats in Kenya by pyrosequencing bacterial 16S rRNA fragments. Immatures and adults showed distinctive gut community structures. Photosynthetic Cyanobacteria were predominant in the larval and pupal guts while Proteobacteria and Bacteroidetes dominated the adult guts, with core taxa of Enterobacteriaceae and Flavobacteriaceae. At the adult stage, diet regime (sugar meal and blood meal) significantly affects the microbial structure. Intriguingly, blood meals drastically reduced the community diversity and favored enteric bacteria. Comparative genomic analysis revealed that the enriched enteric bacteria possess large genetic redox capacity of coping with oxidative and nitrosative stresses that are associated with the catabolism of blood meal, suggesting a beneficial role in maintaining gut redox homeostasis. Interestingly, gut community structure was similar in the adult stage between the field and laboratory mosquitoes, indicating that mosquito gut is a selective eco-environment for its microbiome. This comprehensive gut metatgenomic profile suggests a concerted symbiotic genetic association between gut inhabitants and host.
doi_str_mv 10.1371/journal.pone.0024767
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It is increasingly clear that the gut microbiome influences a wide variety of host traits, such as fitness and immunity. Understanding the microbial community structure and its dynamics across mosquito life is a prerequisite for comprehending the symbiotic relationship between the mosquito and its gut microbial residents. Here we characterized gut bacterial communities across larvae, pupae and adults of Anopheles gambiae reared in semi-natural habitats in Kenya by pyrosequencing bacterial 16S rRNA fragments. Immatures and adults showed distinctive gut community structures. Photosynthetic Cyanobacteria were predominant in the larval and pupal guts while Proteobacteria and Bacteroidetes dominated the adult guts, with core taxa of Enterobacteriaceae and Flavobacteriaceae. At the adult stage, diet regime (sugar meal and blood meal) significantly affects the microbial structure. Intriguingly, blood meals drastically reduced the community diversity and favored enteric bacteria. 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It is increasingly clear that the gut microbiome influences a wide variety of host traits, such as fitness and immunity. Understanding the microbial community structure and its dynamics across mosquito life is a prerequisite for comprehending the symbiotic relationship between the mosquito and its gut microbial residents. Here we characterized gut bacterial communities across larvae, pupae and adults of Anopheles gambiae reared in semi-natural habitats in Kenya by pyrosequencing bacterial 16S rRNA fragments. Immatures and adults showed distinctive gut community structures. Photosynthetic Cyanobacteria were predominant in the larval and pupal guts while Proteobacteria and Bacteroidetes dominated the adult guts, with core taxa of Enterobacteriaceae and Flavobacteriaceae. At the adult stage, diet regime (sugar meal and blood meal) significantly affects the microbial structure. Intriguingly, blood meals drastically reduced the community diversity and favored enteric bacteria. 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Comparative genomic analysis revealed that the enriched enteric bacteria possess large genetic redox capacity of coping with oxidative and nitrosative stresses that are associated with the catabolism of blood meal, suggesting a beneficial role in maintaining gut redox homeostasis. Interestingly, gut community structure was similar in the adult stage between the field and laboratory mosquitoes, indicating that mosquito gut is a selective eco-environment for its microbiome. This comprehensive gut metatgenomic profile suggests a concerted symbiotic genetic association between gut inhabitants and host.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21957459</pmid><doi>10.1371/journal.pone.0024767</doi><tpages>e24767</tpages><oa>free_for_read</oa></addata></record>
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subjects Adults
Analysis
Animal Feed
Animals
Anopheles
Anopheles - growth & development
Anopheles - microbiology
Anopheles gambiae
Antibiotics
Aquatic insects
Bacteria
Bacteria - genetics
Bacteria - isolation & purification
Bacteroidetes
Biodiversity
Biology
Blood
Blood meals
Boophilus
Catabolism
Cattle
Communities
Community structure
Culicidae
Cyanobacteria
Digestive system
Ecosystem biology
Ecosystems
Enterobacteriaceae
Female
Fitness
Gastrointestinal Tract - microbiology
Genomic analysis
Habitats
Homeostasis
Humans
Immunity
Inhabitants
Insect Vectors - growth & development
Insect Vectors - microbiology
Internet resources
Intestinal microflora
Kenya
Laboratories
Larvae
Life Cycle Stages
Life history
Malaria
Malaria - transmission
Meals
Medical research
Medicine
Metagenome
Metagenomics
Microbiota
Microorganisms
Mosquitoes
Oxidation-Reduction
Photosynthesis
Proteobacteria
Public health
Reproductive fitness
Rhipicephalus
RNA, Bacterial - genetics
RNA, Ribosomal, 16S - genetics
rRNA 16S
Sequence Analysis, RNA
Sugar
Taxa
Taxonomy
Vector-borne diseases
title Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya
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