A gene co-association network regulating gut microbial communities in a Duroc pig population

Background: 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 "s...

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Autores: Reverter, Antonio|||0000-0002-4681-9404, Ballester Devis, Maria|||0000-0002-5413-4640, Alexandre, Pamela A., Mármol-Sánchez, Emilio|||0000-0002-4393-1740, Dalmau Bueno, Antoni|||0000-0003-2248-6796, Quintanilla, Raquel|||0000-0003-3274-3434, Ramayo-Caldas, Yuliaxis|||0000-0002-8142-0159
Tipo de recurso: artículo
Fecha de publicación:2021
País:España
Institución:Universitat Autònoma de Barcelona
Repositorio:Dipòsit Digital de Documents de la UAB
Idioma:inglés
OAI Identifier:oai:ddd.uab.cat:237191
Acceso en línea:https://ddd.uab.cat/record/237191
https://dx.doi.org/urn:doi:10.1186/s40168-020-00994-8
Access Level:acceso abierto
Palabra clave:Microbiota
Pig
Gene network
Regulators
Protist
Bacteria
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spelling A gene co-association network regulating gut microbial communities in a Duroc pig populationReverter, Antonio|||0000-0002-4681-9404Ballester Devis, Maria|||0000-0002-5413-4640Alexandre, Pamela A.Mármol-Sánchez, Emilio|||0000-0002-4393-1740Dalmau Bueno, Antoni|||0000-0003-2248-6796Quintanilla, Raquel|||0000-0003-3274-3434Ramayo-Caldas, Yuliaxis|||0000-0002-8142-0159MicrobiotaPigGene networkRegulatorsProtistBacteriaBackground: 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. Results: 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. 22021-01-0120212021-01-01Articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://ddd.uab.cat/record/237191https://dx.doi.org/urn:doi:10.1186/s40168-020-00994-8reponame:Dipòsit Digital de Documents de la UABinstname:Universitat Autònoma de BarcelonaInglésengEuropean Commission https://doi.org/10.13039/501100000780 665919Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 RYC-2013-12573Ministerio de Educación y Ciencia FPU15-01733Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 AGL2016-75432-RAgencia Estatal de Investigación https://doi.org/10.13039/501100011033 AGL2017-88849-RAgència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2017/SGR-1719open accesshttp://purl.org/coar/access_right/c_abf2Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, fins i tot amb finalitats comercials, sempre i quan es reconegui l'autoria de l'obra original.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:ddd.uab.cat:2371912026-06-06T12:50:31Z
dc.title.none.fl_str_mv A gene co-association network regulating gut microbial communities in a Duroc pig population
title A gene co-association network regulating gut microbial communities in a Duroc pig population
spellingShingle A gene co-association network regulating gut microbial communities in a Duroc pig population
Reverter, Antonio|||0000-0002-4681-9404
Microbiota
Pig
Gene network
Regulators
Protist
Bacteria
title_short A gene co-association network regulating gut microbial communities in a Duroc pig population
title_full A gene co-association network regulating gut microbial communities in a Duroc pig population
title_fullStr A gene co-association network regulating gut microbial communities in a Duroc pig population
title_full_unstemmed A gene co-association network regulating gut microbial communities in a Duroc pig population
title_sort A gene co-association network regulating gut microbial communities in a Duroc pig population
dc.creator.none.fl_str_mv Reverter, Antonio|||0000-0002-4681-9404
Ballester Devis, Maria|||0000-0002-5413-4640
Alexandre, Pamela A.
Mármol-Sánchez, Emilio|||0000-0002-4393-1740
Dalmau Bueno, Antoni|||0000-0003-2248-6796
Quintanilla, Raquel|||0000-0003-3274-3434
Ramayo-Caldas, Yuliaxis|||0000-0002-8142-0159
author Reverter, Antonio|||0000-0002-4681-9404
author_facet Reverter, Antonio|||0000-0002-4681-9404
Ballester Devis, Maria|||0000-0002-5413-4640
Alexandre, Pamela A.
Mármol-Sánchez, Emilio|||0000-0002-4393-1740
Dalmau Bueno, Antoni|||0000-0003-2248-6796
Quintanilla, Raquel|||0000-0003-3274-3434
Ramayo-Caldas, Yuliaxis|||0000-0002-8142-0159
author_role author
author2 Ballester Devis, Maria|||0000-0002-5413-4640
Alexandre, Pamela A.
Mármol-Sánchez, Emilio|||0000-0002-4393-1740
Dalmau Bueno, Antoni|||0000-0003-2248-6796
Quintanilla, Raquel|||0000-0003-3274-3434
Ramayo-Caldas, Yuliaxis|||0000-0002-8142-0159
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Microbiota
Pig
Gene network
Regulators
Protist
Bacteria
topic Microbiota
Pig
Gene network
Regulators
Protist
Bacteria
description Background: 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. Results: 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.
publishDate 2021
dc.date.none.fl_str_mv 2
2021-01-01
2021
2021-01-01
dc.type.none.fl_str_mv Article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://ddd.uab.cat/record/237191
https://dx.doi.org/urn:doi:10.1186/s40168-020-00994-8
url https://ddd.uab.cat/record/237191
https://dx.doi.org/urn:doi:10.1186/s40168-020-00994-8
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.relation.none.fl_str_mv European Commission https://doi.org/10.13039/501100000780 665919
Ministerio de Economía y Competitividad https://doi.org/10.13039/501100003329 RYC-2013-12573
Ministerio de Educación y Ciencia FPU15-01733
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 AGL2016-75432-R
Agencia Estatal de Investigación https://doi.org/10.13039/501100011033 AGL2017-88849-R
Agència de Gestió d'Ajuts Universitaris i de Recerca https://doi.org/10.13039/501100003030 2017/SGR-1719
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Dipòsit Digital de Documents de la UAB
instname:Universitat Autònoma de Barcelona
instname_str Universitat Autònoma de Barcelona
reponame_str Dipòsit Digital de Documents de la UAB
collection Dipòsit Digital de Documents de la UAB
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15.300719

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