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A gene co-association network regulating gut microbial communities in a Duroc pig population
Analyses of gut microbiome composition in livestock species have shown its potential to contribute to the regulation of complex phenotypes. However, little is known about the host genetic control over the gut microbial communities. In pigs, previous studies are based on classical "single-gene-s...
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| Published in: | Microbiome 2021-02, Vol.9 (1), p.52-52, Article 52 |
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| creator | Reverter, Antonio Ballester, Maria Alexandre, Pamela A Mármol-Sánchez, Emilio Dalmau, Antoni Quintanilla, Raquel Ramayo-Caldas, Yuliaxis |
| description | Analyses of gut microbiome composition in livestock species have shown its potential to contribute to the regulation of complex phenotypes. However, little is known about the host genetic control over the gut microbial communities. In pigs, previous studies are based on classical "single-gene-single-trait" approaches and have evaluated the role of host genome controlling gut prokaryote and eukaryote communities separately.
In order to determine the ability of the host genome to control the diversity and composition of microbial communities in healthy pigs, we undertook genome-wide association studies (GWAS) for 39 microbial phenotypes that included 2 diversity indexes, and the relative abundance of 31 bacterial and six commensal protist genera in 390 pigs genotyped for 70 K SNPs. The GWAS results were processed through a 3-step analytical pipeline comprised of (1) association weight matrix; (2) regulatory impact factor; and (3) partial correlation and information theory. The inferred gene regulatory network comprised 3561 genes (within a 5 kb distance from a relevant SNP-P |
| doi_str_mv | 10.1186/s40168-020-00994-8 |
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In order to determine the ability of the host genome to control the diversity and composition of microbial communities in healthy pigs, we undertook genome-wide association studies (GWAS) for 39 microbial phenotypes that included 2 diversity indexes, and the relative abundance of 31 bacterial and six commensal protist genera in 390 pigs genotyped for 70 K SNPs. The GWAS results were processed through a 3-step analytical pipeline comprised of (1) association weight matrix; (2) regulatory impact factor; and (3) partial correlation and information theory. The inferred gene regulatory network comprised 3561 genes (within a 5 kb distance from a relevant SNP-P < 0.05) and 738,913 connections (SNP-to-SNP co-associations). Our findings highlight the complexity and polygenic nature of the pig gut microbial ecosystem. Prominent within the network were 5 regulators, PRDM15, STAT1, ssc-mir-371, SOX9 and RUNX2 which gathered 942, 607, 588, 284 and 273 connections, respectively. PRDM15 modulates the transcription of upstream regulators of WNT and MAPK-ERK signaling to safeguard naive pluripotency and regulates the production of Th1- and Th2-type immune response. The signal transducer STAT1 has long been associated with immune processes and was recently identified as a potential regulator of vaccine response to porcine reproductive and respiratory syndrome. The list of regulators was enriched for immune-related pathways, and the list of predicted targets includes candidate genes previously reported as associated with microbiota profile in pigs, mice and human, such as SLIT3, SLC39A8, NOS1, IL1R2, DAB1, TOX3, SPP1, THSD7B, ELF2, PIANP, A2ML1, and IFNAR1. Moreover, we show the existence of host-genetic variants jointly associated with the relative abundance of butyrate producer bacteria and host performance.
Taken together, our results identified regulators, candidate genes, and mechanisms linked with microbiome modulation by the host. They further highlight the value of the proposed analytical pipeline to exploit pleiotropy and the crosstalk between bacteria and protists as significant contributors to host-microbiome interactions and identify genetic markers and candidate genes that can be incorporated in breeding program to improve host-performance and microbial traits. Video Abstract.</description><identifier>ISSN: 2049-2618</identifier><identifier>EISSN: 2049-2618</identifier><identifier>DOI: 10.1186/s40168-020-00994-8</identifier><identifier>PMID: 33612109</identifier><language>eng</language><publisher>England: BioMed Central</publisher><subject>Abundance ; Algorithms ; Animal diseases ; Animals ; Bacteria ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Cbfa-1 protein ; Disabled-1 protein ; Female ; Gastrointestinal Microbiome - genetics ; Gene network ; Gene Regulatory Networks ; Genes ; Genetic control ; Genetic diversity ; Genetic markers ; Genome-Wide Association Study ; Genomes ; Genotype & phenotype ; Hogs ; Immune response ; Impact factors ; Information theory ; Interleukin 1 ; Intestinal microflora ; Livestock ; Lymphocytes T ; Male ; MAP kinase ; Microbiomes ; Microbiota ; MicroRNAs ; Nitric-oxide synthase ; Phenotypes ; Pig ; Pleiotropy ; Polygenic inheritance ; Protist ; Regulators ; Single-nucleotide polymorphism ; Sox9 protein ; Stat1 protein ; Swine - classification ; Swine - genetics ; Swine - microbiology ; Symbiosis - genetics ; Transcription</subject><ispartof>Microbiome, 2021-02, Vol.9 (1), p.52-52, Article 52</ispartof><rights>2021. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c496t-6ca0b6786364152f352792277ad52d3e1d0ac008ef2e72bc7d06db1483e77faa3</citedby><cites>FETCH-LOGICAL-c496t-6ca0b6786364152f352792277ad52d3e1d0ac008ef2e72bc7d06db1483e77faa3</cites><orcidid>0000-0002-8142-0159</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7898758/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2502597825?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33612109$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Reverter, Antonio</creatorcontrib><creatorcontrib>Ballester, Maria</creatorcontrib><creatorcontrib>Alexandre, Pamela A</creatorcontrib><creatorcontrib>Mármol-Sánchez, Emilio</creatorcontrib><creatorcontrib>Dalmau, Antoni</creatorcontrib><creatorcontrib>Quintanilla, Raquel</creatorcontrib><creatorcontrib>Ramayo-Caldas, Yuliaxis</creatorcontrib><title>A gene co-association network regulating gut microbial communities in a Duroc pig population</title><title>Microbiome</title><addtitle>Microbiome</addtitle><description>Analyses of gut microbiome composition in livestock species have shown its potential to contribute to the regulation of complex phenotypes. However, little is known about the host genetic control over the gut microbial communities. In pigs, previous studies are based on classical "single-gene-single-trait" approaches and have evaluated the role of host genome controlling gut prokaryote and eukaryote communities separately.
In order to determine the ability of the host genome to control the diversity and composition of microbial communities in healthy pigs, we undertook genome-wide association studies (GWAS) for 39 microbial phenotypes that included 2 diversity indexes, and the relative abundance of 31 bacterial and six commensal protist genera in 390 pigs genotyped for 70 K SNPs. The GWAS results were processed through a 3-step analytical pipeline comprised of (1) association weight matrix; (2) regulatory impact factor; and (3) partial correlation and information theory. The inferred gene regulatory network comprised 3561 genes (within a 5 kb distance from a relevant SNP-P < 0.05) and 738,913 connections (SNP-to-SNP co-associations). Our findings highlight the complexity and polygenic nature of the pig gut microbial ecosystem. Prominent within the network were 5 regulators, PRDM15, STAT1, ssc-mir-371, SOX9 and RUNX2 which gathered 942, 607, 588, 284 and 273 connections, respectively. PRDM15 modulates the transcription of upstream regulators of WNT and MAPK-ERK signaling to safeguard naive pluripotency and regulates the production of Th1- and Th2-type immune response. The signal transducer STAT1 has long been associated with immune processes and was recently identified as a potential regulator of vaccine response to porcine reproductive and respiratory syndrome. The list of regulators was enriched for immune-related pathways, and the list of predicted targets includes candidate genes previously reported as associated with microbiota profile in pigs, mice and human, such as SLIT3, SLC39A8, NOS1, IL1R2, DAB1, TOX3, SPP1, THSD7B, ELF2, PIANP, A2ML1, and IFNAR1. Moreover, we show the existence of host-genetic variants jointly associated with the relative abundance of butyrate producer bacteria and host performance.
Taken together, our results identified regulators, candidate genes, and mechanisms linked with microbiome modulation by the host. They further highlight the value of the proposed analytical pipeline to exploit pleiotropy and the crosstalk between bacteria and protists as significant contributors to host-microbiome interactions and identify genetic markers and candidate genes that can be incorporated in breeding program to improve host-performance and microbial traits. Video Abstract.</description><subject>Abundance</subject><subject>Algorithms</subject><subject>Animal diseases</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Cbfa-1 protein</subject><subject>Disabled-1 protein</subject><subject>Female</subject><subject>Gastrointestinal Microbiome - genetics</subject><subject>Gene network</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genetic control</subject><subject>Genetic diversity</subject><subject>Genetic markers</subject><subject>Genome-Wide Association Study</subject><subject>Genomes</subject><subject>Genotype & phenotype</subject><subject>Hogs</subject><subject>Immune response</subject><subject>Impact factors</subject><subject>Information theory</subject><subject>Interleukin 1</subject><subject>Intestinal microflora</subject><subject>Livestock</subject><subject>Lymphocytes T</subject><subject>Male</subject><subject>MAP kinase</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>MicroRNAs</subject><subject>Nitric-oxide synthase</subject><subject>Phenotypes</subject><subject>Pig</subject><subject>Pleiotropy</subject><subject>Polygenic inheritance</subject><subject>Protist</subject><subject>Regulators</subject><subject>Single-nucleotide polymorphism</subject><subject>Sox9 protein</subject><subject>Stat1 protein</subject><subject>Swine - classification</subject><subject>Swine - genetics</subject><subject>Swine - microbiology</subject><subject>Symbiosis - genetics</subject><subject>Transcription</subject><issn>2049-2618</issn><issn>2049-2618</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNpdkstu1TAQhiMEolXpC7BAltiwCdjj-wapKrdKlbppd0iW4zjBh8QOdgLi7XHPKVVbb2zN_PNpZvw3zWuC3xOixIfCMBGqxYBbjLVmrXrWHANmugVB1PMH76PmtJQdrkcTJpl62RxRKggQrI-b72do9NEjl1pbSnLBriFFFP36J-WfKPtxm2oojmjcVjQHl1MX7FT187zFsAZfUIjIok9bTg4tYURLWvY1Kb5qXgx2Kv707j5pbr58vj7_1l5efb04P7tsHdNibYWzuBNSCSoY4TBQDlIDSGl7Dj31pMfWYaz8AF5C52SPRd8RpqiXcrCWnjQXB26f7M4sOcw2_zXJBrMPpDwam9fgJm-w7CjrmCAD7xijogNNBWbceujtMLjK-nhgLVs3-975uGY7PYI-zsTww4zpt5FKK8lVBby7A-T0a_NlNXMozk-TjT5txQCrsynBKFTp2yfSXdpyrKsywDFwLRXwqoKDqu6-lOyH-2YINrdeMAcvmOoFs_eCue3izcMx7kv-_zz9BzdSr5I</recordid><startdate>20210221</startdate><enddate>20210221</enddate><creator>Reverter, Antonio</creator><creator>Ballester, Maria</creator><creator>Alexandre, Pamela A</creator><creator>Mármol-Sánchez, Emilio</creator><creator>Dalmau, Antoni</creator><creator>Quintanilla, Raquel</creator><creator>Ramayo-Caldas, Yuliaxis</creator><general>BioMed Central</general><general>BMC</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-8142-0159</orcidid></search><sort><creationdate>20210221</creationdate><title>A gene co-association network regulating gut microbial communities in a Duroc pig population</title><author>Reverter, Antonio ; Ballester, Maria ; Alexandre, Pamela A ; Mármol-Sánchez, Emilio ; Dalmau, Antoni ; Quintanilla, Raquel ; Ramayo-Caldas, Yuliaxis</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c496t-6ca0b6786364152f352792277ad52d3e1d0ac008ef2e72bc7d06db1483e77faa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abundance</topic><topic>Algorithms</topic><topic>Animal diseases</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacteria - classification</topic><topic>Bacteria - genetics</topic><topic>Bacteria - isolation & purification</topic><topic>Cbfa-1 protein</topic><topic>Disabled-1 protein</topic><topic>Female</topic><topic>Gastrointestinal Microbiome - genetics</topic><topic>Gene network</topic><topic>Gene Regulatory Networks</topic><topic>Genes</topic><topic>Genetic control</topic><topic>Genetic diversity</topic><topic>Genetic markers</topic><topic>Genome-Wide Association Study</topic><topic>Genomes</topic><topic>Genotype & phenotype</topic><topic>Hogs</topic><topic>Immune response</topic><topic>Impact factors</topic><topic>Information theory</topic><topic>Interleukin 1</topic><topic>Intestinal microflora</topic><topic>Livestock</topic><topic>Lymphocytes T</topic><topic>Male</topic><topic>MAP kinase</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>MicroRNAs</topic><topic>Nitric-oxide synthase</topic><topic>Phenotypes</topic><topic>Pig</topic><topic>Pleiotropy</topic><topic>Polygenic inheritance</topic><topic>Protist</topic><topic>Regulators</topic><topic>Single-nucleotide polymorphism</topic><topic>Sox9 protein</topic><topic>Stat1 protein</topic><topic>Swine - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Microbiome</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Reverter, Antonio</au><au>Ballester, Maria</au><au>Alexandre, Pamela A</au><au>Mármol-Sánchez, Emilio</au><au>Dalmau, Antoni</au><au>Quintanilla, Raquel</au><au>Ramayo-Caldas, Yuliaxis</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A gene co-association network regulating gut microbial communities in a Duroc pig population</atitle><jtitle>Microbiome</jtitle><addtitle>Microbiome</addtitle><date>2021-02-21</date><risdate>2021</risdate><volume>9</volume><issue>1</issue><spage>52</spage><epage>52</epage><pages>52-52</pages><artnum>52</artnum><issn>2049-2618</issn><eissn>2049-2618</eissn><abstract>Analyses of gut microbiome composition in livestock species have shown its potential to contribute to the regulation of complex phenotypes. However, little is known about the host genetic control over the gut microbial communities. In pigs, previous studies are based on classical "single-gene-single-trait" approaches and have evaluated the role of host genome controlling gut prokaryote and eukaryote communities separately.
In order to determine the ability of the host genome to control the diversity and composition of microbial communities in healthy pigs, we undertook genome-wide association studies (GWAS) for 39 microbial phenotypes that included 2 diversity indexes, and the relative abundance of 31 bacterial and six commensal protist genera in 390 pigs genotyped for 70 K SNPs. The GWAS results were processed through a 3-step analytical pipeline comprised of (1) association weight matrix; (2) regulatory impact factor; and (3) partial correlation and information theory. The inferred gene regulatory network comprised 3561 genes (within a 5 kb distance from a relevant SNP-P < 0.05) and 738,913 connections (SNP-to-SNP co-associations). Our findings highlight the complexity and polygenic nature of the pig gut microbial ecosystem. Prominent within the network were 5 regulators, PRDM15, STAT1, ssc-mir-371, SOX9 and RUNX2 which gathered 942, 607, 588, 284 and 273 connections, respectively. PRDM15 modulates the transcription of upstream regulators of WNT and MAPK-ERK signaling to safeguard naive pluripotency and regulates the production of Th1- and Th2-type immune response. The signal transducer STAT1 has long been associated with immune processes and was recently identified as a potential regulator of vaccine response to porcine reproductive and respiratory syndrome. The list of regulators was enriched for immune-related pathways, and the list of predicted targets includes candidate genes previously reported as associated with microbiota profile in pigs, mice and human, such as SLIT3, SLC39A8, NOS1, IL1R2, DAB1, TOX3, SPP1, THSD7B, ELF2, PIANP, A2ML1, and IFNAR1. Moreover, we show the existence of host-genetic variants jointly associated with the relative abundance of butyrate producer bacteria and host performance.
Taken together, our results identified regulators, candidate genes, and mechanisms linked with microbiome modulation by the host. They further highlight the value of the proposed analytical pipeline to exploit pleiotropy and the crosstalk between bacteria and protists as significant contributors to host-microbiome interactions and identify genetic markers and candidate genes that can be incorporated in breeding program to improve host-performance and microbial traits. Video Abstract.</abstract><cop>England</cop><pub>BioMed Central</pub><pmid>33612109</pmid><doi>10.1186/s40168-020-00994-8</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-8142-0159</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Abundance Algorithms Animal diseases Animals Bacteria Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Cbfa-1 protein Disabled-1 protein Female Gastrointestinal Microbiome - genetics Gene network Gene Regulatory Networks Genes Genetic control Genetic diversity Genetic markers Genome-Wide Association Study Genomes Genotype & phenotype Hogs Immune response Impact factors Information theory Interleukin 1 Intestinal microflora Livestock Lymphocytes T Male MAP kinase Microbiomes Microbiota MicroRNAs Nitric-oxide synthase Phenotypes Pig Pleiotropy Polygenic inheritance Protist Regulators Single-nucleotide polymorphism Sox9 protein Stat1 protein Swine - classification Swine - genetics Swine - microbiology Symbiosis - genetics Transcription |
| title | A gene co-association network regulating gut microbial communities in a Duroc pig population |
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