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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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. |
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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. 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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0024767</identifier><identifier>PMID: 21957459</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>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</subject><ispartof>PloS one, 2011-09, Vol.6 (9), p.e24767-e24767</ispartof><rights>COPYRIGHT 2011 Public Library of Science</rights><rights>2011 Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Wang et al. 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c640t-91fa78f6b3780c2be82c46595a6bbff82d1d68224481aaaf75b964daff1f84b53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3177825/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3177825/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53770,53772,79347,79348</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21957459$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Leulier, François</contributor><creatorcontrib>Wang, Ying</creatorcontrib><creatorcontrib>Gilbreath, 3rd, Thomas M</creatorcontrib><creatorcontrib>Kukutla, Phanidhar</creatorcontrib><creatorcontrib>Yan, Guiyun</creatorcontrib><creatorcontrib>Xu, Jiannong</creatorcontrib><title>Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya</title><title>PloS one</title><addtitle>PLoS One</addtitle><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.</description><subject>Adults</subject><subject>Analysis</subject><subject>Animal Feed</subject><subject>Animals</subject><subject>Anopheles</subject><subject>Anopheles - growth & development</subject><subject>Anopheles - microbiology</subject><subject>Anopheles gambiae</subject><subject>Antibiotics</subject><subject>Aquatic insects</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteroidetes</subject><subject>Biodiversity</subject><subject>Biology</subject><subject>Blood</subject><subject>Blood meals</subject><subject>Boophilus</subject><subject>Catabolism</subject><subject>Cattle</subject><subject>Communities</subject><subject>Community structure</subject><subject>Culicidae</subject><subject>Cyanobacteria</subject><subject>Digestive system</subject><subject>Ecosystem biology</subject><subject>Ecosystems</subject><subject>Enterobacteriaceae</subject><subject>Female</subject><subject>Fitness</subject><subject>Gastrointestinal Tract - microbiology</subject><subject>Genomic analysis</subject><subject>Habitats</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>Immunity</subject><subject>Inhabitants</subject><subject>Insect Vectors - growth & development</subject><subject>Insect Vectors - microbiology</subject><subject>Internet resources</subject><subject>Intestinal microflora</subject><subject>Kenya</subject><subject>Laboratories</subject><subject>Larvae</subject><subject>Life Cycle Stages</subject><subject>Life history</subject><subject>Malaria</subject><subject>Malaria - transmission</subject><subject>Meals</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Metagenome</subject><subject>Metagenomics</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Mosquitoes</subject><subject>Oxidation-Reduction</subject><subject>Photosynthesis</subject><subject>Proteobacteria</subject><subject>Public health</subject><subject>Reproductive fitness</subject><subject>Rhipicephalus</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>rRNA 16S</subject><subject>Sequence Analysis, RNA</subject><subject>Sugar</subject><subject>Taxa</subject><subject>Taxonomy</subject><subject>Vector-borne diseases</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1uL1DAUx4so7rr6DUQDguLDjM2tTV8WhvU2uLDg7U3CaZu0GdJmtknF-fZmdrrLVPZB8nBC8jv_nJxLkjzH6RLTHL_buHHowS63rlfLNCUsz_IHySkuKFlkJKUPj_YnyRPvN2nKqciyx8kJwQXPGS9Ok1_vdz10pkLNGFC0gyuN6xSCuPMeWaMVao0Pbtghp1FoFerAwmAAdc5fjyY4tOrdtlVWedRAVxpQyPToi-p38DR5pMF69WyyZ8mPjx--X3xeXF59Wl-sLhdVxtKwKLCGXOispLlIK1IqQSqW8YJDVpZaC1LjOhOEMCYwAOicl0XGatAaa8FKTs-SlwfdrXVeTpnxEtNUMJ5RUkRifSBqBxu5HUwHw046MPLmwA2NhCGYyiopOKuFYhWBImWKFqLiFS0UA85FKXIWtc6n18ayU3Wl-jCAnYnOb3rTysb9lhTnuSD7cN9MAoO7HpUPsjO-UtZCr9zopSh4DCLnJJKv_iHv_9xENRDjN7128dlqrylXsS1EzCoXkVreQ8VVq1j42EXaxPOZw9uZQ2SC-hMaGL2X629f_5-9-jlnXx-xrQIbWu_sGIzr_RxkB_CmGQel73KMU7kfgttsyP0QyGkIotuL4_rcOd12Pf0LTKcCHQ</recordid><startdate>20110921</startdate><enddate>20110921</enddate><creator>Wang, Ying</creator><creator>Gilbreath, 3rd, Thomas M</creator><creator>Kukutla, Phanidhar</creator><creator>Yan, Guiyun</creator><creator>Xu, Jiannong</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20110921</creationdate><title>Dynamic gut microbiome across life history of the malaria mosquito Anopheles gambiae in Kenya</title><author>Wang, Ying ; Gilbreath, 3rd, Thomas M ; Kukutla, Phanidhar ; Yan, Guiyun ; Xu, Jiannong</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c640t-91fa78f6b3780c2be82c46595a6bbff82d1d68224481aaaf75b964daff1f84b53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Adults</topic><topic>Analysis</topic><topic>Animal Feed</topic><topic>Animals</topic><topic>Anopheles</topic><topic>Anopheles - growth & development</topic><topic>Anopheles - microbiology</topic><topic>Anopheles gambiae</topic><topic>Antibiotics</topic><topic>Aquatic insects</topic><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Bacteria - isolation & purification</topic><topic>Bacteroidetes</topic><topic>Biodiversity</topic><topic>Biology</topic><topic>Blood</topic><topic>Blood meals</topic><topic>Boophilus</topic><topic>Catabolism</topic><topic>Cattle</topic><topic>Communities</topic><topic>Community structure</topic><topic>Culicidae</topic><topic>Cyanobacteria</topic><topic>Digestive system</topic><topic>Ecosystem biology</topic><topic>Ecosystems</topic><topic>Enterobacteriaceae</topic><topic>Female</topic><topic>Fitness</topic><topic>Gastrointestinal Tract - microbiology</topic><topic>Genomic analysis</topic><topic>Habitats</topic><topic>Homeostasis</topic><topic>Humans</topic><topic>Immunity</topic><topic>Inhabitants</topic><topic>Insect Vectors - growth & development</topic><topic>Insect Vectors - 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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. 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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-21T11%3A00%3A13IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Dynamic%20gut%20microbiome%20across%20life%20history%20of%20the%20malaria%20mosquito%20Anopheles%20gambiae%20in%20Kenya&rft.jtitle=PloS%20one&rft.au=Wang,%20Ying&rft.date=2011-09-21&rft.volume=6&rft.issue=9&rft.spage=e24767&rft.epage=e24767&rft.pages=e24767-e24767&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0024767&rft_dat=%3Cgale_plos_%3EA476878058%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1308456329&rft_id=info:pmid/21957459&rft_galeid=A476878058&rft_doaj_id=oai_doaj_org_article_854d8e4c2a904e398c5c39e4a558b874&rfr_iscdi=true |