Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits
The gastrointestinal tract harbors a complex and diverse microbiota that has an important role in host metabolism. Microbial diversity is influenced by a combination of environmental and host genetic factors and is associated with several polygenic diseases. In this study we combined next-generation...
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| Veröffentlicht in: | PloS one 2012-06, Vol.7 (6), p.e39191-e39191 |
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| creator | McKnite, Autumn M Perez-Munoz, Maria Elisa Lu, Lu Williams, Evan G Brewer, Simon Andreux, Pénélope A Bastiaansen, John W M Wang, Xusheng Kachman, Stephen D Auwerx, Johan Williams, Robert W Benson, Andrew K Peterson, Daniel A Ciobanu, Daniel C |
| description | The gastrointestinal tract harbors a complex and diverse microbiota that has an important role in host metabolism. Microbial diversity is influenced by a combination of environmental and host genetic factors and is associated with several polygenic diseases. In this study we combined next-generation sequencing, genetic mapping, and a set of physiological traits of the BXD mouse population to explore genetic factors that explain differences in gut microbiota and its impact on metabolic traits. Molecular profiling of the gut microbiota revealed important quantitative differences in microbial composition among BXD strains. These differences in gut microbial composition are influenced by host-genetics, which is complex and involves many loci. Linkage analysis defined Quantitative Trait Loci (QTLs) restricted to a particular taxon, branch or that influenced the variation of taxa across phyla. Gene expression within the gastrointestinal tract and sequence analysis of the parental genomes in the QTL regions uncovered candidate genes with potential to alter gut immunological profiles and impact the balance between gut microbial communities. A QTL region on Chr 4 that overlaps several interferon genes modulates the population of Bacteroides, and potentially Bacteroidetes and Firmicutes-the predominant BXD gut phyla. Irak4, a signaling molecule in the Toll-like receptor pathways is a candidate for the QTL on Chr15 that modulates Rikenellaceae, whereas Tgfb3, a cytokine modulating the barrier function of the intestine and tolerance to commensal bacteria, overlaps a QTL on Chr 12 that influence Prevotellaceae. Relationships between gut microflora, morphological and metabolic traits were uncovered, some potentially a result of common genetic sources of variation. |
| doi_str_mv | 10.1371/journal.pone.0039191 |
| format | Article |
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Microbial diversity is influenced by a combination of environmental and host genetic factors and is associated with several polygenic diseases. In this study we combined next-generation sequencing, genetic mapping, and a set of physiological traits of the BXD mouse population to explore genetic factors that explain differences in gut microbiota and its impact on metabolic traits. Molecular profiling of the gut microbiota revealed important quantitative differences in microbial composition among BXD strains. These differences in gut microbial composition are influenced by host-genetics, which is complex and involves many loci. Linkage analysis defined Quantitative Trait Loci (QTLs) restricted to a particular taxon, branch or that influenced the variation of taxa across phyla. Gene expression within the gastrointestinal tract and sequence analysis of the parental genomes in the QTL regions uncovered candidate genes with potential to alter gut immunological profiles and impact the balance between gut microbial communities. A QTL region on Chr 4 that overlaps several interferon genes modulates the population of Bacteroides, and potentially Bacteroidetes and Firmicutes-the predominant BXD gut phyla. Irak4, a signaling molecule in the Toll-like receptor pathways is a candidate for the QTL on Chr15 that modulates Rikenellaceae, whereas Tgfb3, a cytokine modulating the barrier function of the intestine and tolerance to commensal bacteria, overlaps a QTL on Chr 12 that influence Prevotellaceae. Relationships between gut microflora, morphological and metabolic traits were uncovered, some potentially a result of common genetic sources of variation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0039191</identifier><identifier>PMID: 22723961</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Anatomy & physiology ; Animal sciences ; Animals ; Bacteria ; Bacteroidaceae - classification ; Bacteroidaceae - genetics ; Bacteroidetes ; Biological response modifiers ; Biology ; chain fatty-acids ; Chromosome Mapping ; Chromosomes, Mammalian ; diet ; Digestive system ; Digestive tract ; expression ; Firmicutes ; Food science ; Gastrointestinal system ; Gastrointestinal tract ; Gene expression ; Gene mapping ; Gene sequencing ; Gene-Environment Interaction ; Genes ; Genetic aspects ; Genetic diversity ; Genetic factors ; Genetic Variation ; Genetics ; genome-wide association ; Genome-Wide Association Study ; Genomes ; Genomics ; Host-Pathogen Interactions ; House mouse ; Immunological tolerance ; Immunology ; inbred mouse strains ; induced obesity ; innate immunity ; Interferon ; Intestinal microflora ; Intestine ; Intestines - microbiology ; Laboratories ; Lactobacillus ; Linkage analysis ; Loci ; Metabolism ; Metagenome ; Mice ; Microbial activity ; Microbiota ; Microbiota (Symbiotic organisms) ; Microorganisms ; Neurobiology ; Neurosciences ; Obesity ; Pathogens ; Physiological aspects ; Physiological effects ; Physiology ; Polygenic inheritance ; Population ; Population genetics ; Quantitative genetics ; Quantitative Trait Loci ; Signaling ; Studies ; Taxa ; Toll-like receptors ; Variation ; weight ; Zoology</subject><ispartof>PloS one, 2012-06, Vol.7 (6), p.e39191-e39191</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 McKnite 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>McKnite et al. 2012</rights><rights>Wageningen University & Research</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c860t-d7851e66205ea09a2bdebff8b849ab2bf70f96dd5546e0f7654b221f4680e2803</citedby><cites>FETCH-LOGICAL-c860t-d7851e66205ea09a2bdebff8b849ab2bf70f96dd5546e0f7654b221f4680e2803</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/PMC3377628/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3377628/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22723961$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>White, Bryan A.</contributor><creatorcontrib>McKnite, Autumn M</creatorcontrib><creatorcontrib>Perez-Munoz, Maria Elisa</creatorcontrib><creatorcontrib>Lu, Lu</creatorcontrib><creatorcontrib>Williams, Evan G</creatorcontrib><creatorcontrib>Brewer, Simon</creatorcontrib><creatorcontrib>Andreux, Pénélope A</creatorcontrib><creatorcontrib>Bastiaansen, John W M</creatorcontrib><creatorcontrib>Wang, Xusheng</creatorcontrib><creatorcontrib>Kachman, Stephen D</creatorcontrib><creatorcontrib>Auwerx, Johan</creatorcontrib><creatorcontrib>Williams, Robert W</creatorcontrib><creatorcontrib>Benson, Andrew K</creatorcontrib><creatorcontrib>Peterson, Daniel A</creatorcontrib><creatorcontrib>Ciobanu, Daniel C</creatorcontrib><title>Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The gastrointestinal tract harbors a complex and diverse microbiota that has an important role in host metabolism. Microbial diversity is influenced by a combination of environmental and host genetic factors and is associated with several polygenic diseases. In this study we combined next-generation sequencing, genetic mapping, and a set of physiological traits of the BXD mouse population to explore genetic factors that explain differences in gut microbiota and its impact on metabolic traits. Molecular profiling of the gut microbiota revealed important quantitative differences in microbial composition among BXD strains. These differences in gut microbial composition are influenced by host-genetics, which is complex and involves many loci. Linkage analysis defined Quantitative Trait Loci (QTLs) restricted to a particular taxon, branch or that influenced the variation of taxa across phyla. Gene expression within the gastrointestinal tract and sequence analysis of the parental genomes in the QTL regions uncovered candidate genes with potential to alter gut immunological profiles and impact the balance between gut microbial communities. A QTL region on Chr 4 that overlaps several interferon genes modulates the population of Bacteroides, and potentially Bacteroidetes and Firmicutes-the predominant BXD gut phyla. Irak4, a signaling molecule in the Toll-like receptor pathways is a candidate for the QTL on Chr15 that modulates Rikenellaceae, whereas Tgfb3, a cytokine modulating the barrier function of the intestine and tolerance to commensal bacteria, overlaps a QTL on Chr 12 that influence Prevotellaceae. Relationships between gut microflora, morphological and metabolic traits were uncovered, some potentially a result of common genetic sources of variation.</description><subject>Analysis</subject><subject>Anatomy & physiology</subject><subject>Animal sciences</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacteroidaceae - classification</subject><subject>Bacteroidaceae - genetics</subject><subject>Bacteroidetes</subject><subject>Biological response modifiers</subject><subject>Biology</subject><subject>chain fatty-acids</subject><subject>Chromosome Mapping</subject><subject>Chromosomes, Mammalian</subject><subject>diet</subject><subject>Digestive system</subject><subject>Digestive tract</subject><subject>expression</subject><subject>Firmicutes</subject><subject>Food science</subject><subject>Gastrointestinal system</subject><subject>Gastrointestinal tract</subject><subject>Gene expression</subject><subject>Gene mapping</subject><subject>Gene sequencing</subject><subject>Gene-Environment Interaction</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic diversity</subject><subject>Genetic factors</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>genome-wide association</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Host-Pathogen Interactions</subject><subject>House mouse</subject><subject>Immunological tolerance</subject><subject>Immunology</subject><subject>inbred mouse strains</subject><subject>induced obesity</subject><subject>innate immunity</subject><subject>Interferon</subject><subject>Intestinal microflora</subject><subject>Intestine</subject><subject>Intestines - microbiology</subject><subject>Laboratories</subject><subject>Lactobacillus</subject><subject>Linkage analysis</subject><subject>Loci</subject><subject>Metabolism</subject><subject>Metagenome</subject><subject>Mice</subject><subject>Microbial activity</subject><subject>Microbiota</subject><subject>Microbiota (Symbiotic organisms)</subject><subject>Microorganisms</subject><subject>Neurobiology</subject><subject>Neurosciences</subject><subject>Obesity</subject><subject>Pathogens</subject><subject>Physiological aspects</subject><subject>Physiological effects</subject><subject>Physiology</subject><subject>Polygenic inheritance</subject><subject>Population</subject><subject>Population genetics</subject><subject>Quantitative genetics</subject><subject>Quantitative Trait Loci</subject><subject>Signaling</subject><subject>Studies</subject><subject>Taxa</subject><subject>Toll-like 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gut microbiota is defined by host genetics and modulates variation of metabolic traits</title><author>McKnite, Autumn M ; Perez-Munoz, Maria Elisa ; Lu, Lu ; Williams, Evan G ; Brewer, Simon ; Andreux, Pénélope A ; Bastiaansen, John W M ; Wang, Xusheng ; Kachman, Stephen D ; Auwerx, Johan ; Williams, Robert W ; Benson, Andrew K ; Peterson, Daniel A ; Ciobanu, Daniel C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c860t-d7851e66205ea09a2bdebff8b849ab2bf70f96dd5546e0f7654b221f4680e2803</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Analysis</topic><topic>Anatomy & physiology</topic><topic>Animal sciences</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacteroidaceae - classification</topic><topic>Bacteroidaceae - genetics</topic><topic>Bacteroidetes</topic><topic>Biological response modifiers</topic><topic>Biology</topic><topic>chain 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Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>NARCIS:Publications</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>McKnite, Autumn M</au><au>Perez-Munoz, Maria Elisa</au><au>Lu, Lu</au><au>Williams, Evan G</au><au>Brewer, Simon</au><au>Andreux, Pénélope A</au><au>Bastiaansen, John W M</au><au>Wang, Xusheng</au><au>Kachman, Stephen D</au><au>Auwerx, Johan</au><au>Williams, Robert W</au><au>Benson, Andrew K</au><au>Peterson, Daniel A</au><au>Ciobanu, Daniel C</au><au>White, Bryan A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2012-06-18</date><risdate>2012</risdate><volume>7</volume><issue>6</issue><spage>e39191</spage><epage>e39191</epage><pages>e39191-e39191</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The gastrointestinal tract harbors a complex and diverse microbiota that has an important role in host metabolism. Microbial diversity is influenced by a combination of environmental and host genetic factors and is associated with several polygenic diseases. In this study we combined next-generation sequencing, genetic mapping, and a set of physiological traits of the BXD mouse population to explore genetic factors that explain differences in gut microbiota and its impact on metabolic traits. Molecular profiling of the gut microbiota revealed important quantitative differences in microbial composition among BXD strains. These differences in gut microbial composition are influenced by host-genetics, which is complex and involves many loci. Linkage analysis defined Quantitative Trait Loci (QTLs) restricted to a particular taxon, branch or that influenced the variation of taxa across phyla. Gene expression within the gastrointestinal tract and sequence analysis of the parental genomes in the QTL regions uncovered candidate genes with potential to alter gut immunological profiles and impact the balance between gut microbial communities. A QTL region on Chr 4 that overlaps several interferon genes modulates the population of Bacteroides, and potentially Bacteroidetes and Firmicutes-the predominant BXD gut phyla. Irak4, a signaling molecule in the Toll-like receptor pathways is a candidate for the QTL on Chr15 that modulates Rikenellaceae, whereas Tgfb3, a cytokine modulating the barrier function of the intestine and tolerance to commensal bacteria, overlaps a QTL on Chr 12 that influence Prevotellaceae. Relationships between gut microflora, morphological and metabolic traits were uncovered, some potentially a result of common genetic sources of variation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22723961</pmid><doi>10.1371/journal.pone.0039191</doi><tpages>e39191</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2012-06, Vol.7 (6), p.e39191-e39191 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1326201061 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Analysis Anatomy & physiology Animal sciences Animals Bacteria Bacteroidaceae - classification Bacteroidaceae - genetics Bacteroidetes Biological response modifiers Biology chain fatty-acids Chromosome Mapping Chromosomes, Mammalian diet Digestive system Digestive tract expression Firmicutes Food science Gastrointestinal system Gastrointestinal tract Gene expression Gene mapping Gene sequencing Gene-Environment Interaction Genes Genetic aspects Genetic diversity Genetic factors Genetic Variation Genetics genome-wide association Genome-Wide Association Study Genomes Genomics Host-Pathogen Interactions House mouse Immunological tolerance Immunology inbred mouse strains induced obesity innate immunity Interferon Intestinal microflora Intestine Intestines - microbiology Laboratories Lactobacillus Linkage analysis Loci Metabolism Metagenome Mice Microbial activity Microbiota Microbiota (Symbiotic organisms) Microorganisms Neurobiology Neurosciences Obesity Pathogens Physiological aspects Physiological effects Physiology Polygenic inheritance Population Population genetics Quantitative genetics Quantitative Trait Loci Signaling Studies Taxa Toll-like receptors Variation weight Zoology |
| title | Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits |
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