Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome

Background High-throughput sequencing technologies play an increasingly active role in the surveillance of major global health challenges, such as the emergence of antimicrobial resistance. The post-weaning period is of critical importance for the swine industry and antimicrobials are still required...

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Autores: Guitart-Matas, Judith, Vera-Ponce de León, Arturo, Pope, Phillip B., Hvidsten, Torgeir R., Fraile, Lorenzo, Ballester Devis, Maria, Ramayo-Caldas, Yuliaxis, Migura, Lourdes
Tipo de recurso: artículo
Fecha de publicación:2025
País:España
Institución:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
Repositorio:IRTA Pubpro. Open Digital Archive
OAI Identifier:oai:repositori.irta.cat:20.500.12327/4689
Acceso en línea:http://hdl.handle.net/20.500.12327/4689
https://doi.org/10.1186/s42523-025-00418-8
Access Level:acceso abierto
Palabra clave:619
id ES_ebd21e9dd7b8cd7e90c2900f5d2ea6ae
oai_identifier_str oai:repositori.irta.cat:20.500.12327/4689
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
title Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
spellingShingle Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
Guitart-Matas, Judith
619
title_short Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
title_full Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
title_fullStr Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
title_full_unstemmed Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
title_sort Multi-omics surveillance of antimicrobial resistance in the pig gut microbiome
dc.creator.none.fl_str_mv Guitart-Matas, Judith
Vera-Ponce de León, Arturo
Pope, Phillip B.
Hvidsten, Torgeir R.
Fraile, Lorenzo
Ballester Devis, Maria
Ramayo-Caldas, Yuliaxis
Migura, Lourdes
author Guitart-Matas, Judith
author_facet Guitart-Matas, Judith
Vera-Ponce de León, Arturo
Pope, Phillip B.
Hvidsten, Torgeir R.
Fraile, Lorenzo
Ballester Devis, Maria
Ramayo-Caldas, Yuliaxis
Migura, Lourdes
author_role author
author2 Vera-Ponce de León, Arturo
Pope, Phillip B.
Hvidsten, Torgeir R.
Fraile, Lorenzo
Ballester Devis, Maria
Ramayo-Caldas, Yuliaxis
Migura, Lourdes
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Producció Animal
Sanitat Animal
Genètica i Millora Animal
dc.subject.none.fl_str_mv 619
topic 619
description Background High-throughput sequencing technologies play an increasingly active role in the surveillance of major global health challenges, such as the emergence of antimicrobial resistance. The post-weaning period is of critical importance for the swine industry and antimicrobials are still required when infection occurs during this period. Here, two sequencing approaches, shotgun metagenomics and metatranscriptomics, have been applied to decipher the effect of different treatments used in post-weaning diarrhea on the transcriptome and resistome of pig gut microbiome. With this objective, a metagenome-assembled genome (MAG) catalogue was generated to use as a reference database for transcript mapping obtained from a total of 140 pig fecal samples in a cross-sectional and longitudinal design to study differential gene expression. The different treatments included antimicrobials trimethoprim/sulfamethoxazole, colistin, gentamicin, and amoxicillin, and an oral commercial vaccine, a control with water acidification, and an untreated control. For metatranscriptomics, fecal samples from pigs were selected before weaning, three days and four weeks post-treatment. Results The final non-redundant MAGs collection comprised a total of 1396 genomes obtained from single assemblies and co-assemblies per treatment group and sampling time from the metagenomics data. Analysis of antimicrobial resistance genes (ARGs) at this assembly level considerably reduced the total number of ARGs identified in comparison to those found at the reads level. Besides, from the metatranscriptomics data, half of those ARGs were detected transcriptionally active in all treatment groups. Differential gene expression between sampling times after treatment found major number of differential expressed genes (DEGs) against the group treated continuously with amoxicillin, with DEGs being correlated with antimicrobial resistance. Moreover, at three days post-treatment, a high number of significantly downregulated genes was detected in the group treated with gentamicin. At this sampling time, this group showed an altered expression of ribosomal-related genes, demonstrating the rapid effect of gentamicin to inhibit bacterial protein synthesis. Conclusions Different antimicrobial treatments can impact differently the transcriptome and resistome of microbial communities, highlighting the relevance of novel sequencing approaches to monitor the resistome and contribute to a more efficient antimicrobial stewardship.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12327/4689
https://doi.org/10.1186/s42523-025-00418-8
url http://hdl.handle.net/20.500.12327/4689
https://doi.org/10.1186/s42523-025-00418-8
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Animal Microbiome
MICIU/Programa Estatal de I+D+I orientada a los retos de la sociedad/RTI2018-095586-B-C22/ES/OPTIMIZATION OF DIAGNOSIS AND TREATMENT OF POSTWEANING DIARRHEAS IN PIGS: TOWARDS A RATIONAL USE OF ANTIBIOTICS/
MICIU/Programa Estatal de promoción del talento y su empleabilidad en I+D+I/RYC2019-027244-I/ES/Metagenomics and integrative biology tools to improve sustainable livestock systems/
dc.rights.none.fl_str_mv Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 16
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv reponame:IRTA Pubpro. Open Digital Archive
instname:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
instname_str Institut de Recerca i Tecnologia Agroalimentàries (IRTA)
reponame_str IRTA Pubpro. Open Digital Archive
collection IRTA Pubpro. Open Digital Archive
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Multi-omics surveillance of antimicrobial resistance in the pig gut microbiomeGuitart-Matas, JudithVera-Ponce de León, ArturoPope, Phillip B.Hvidsten, Torgeir R.Fraile, LorenzoBallester Devis, MariaRamayo-Caldas, YuliaxisMigura, Lourdes619Background High-throughput sequencing technologies play an increasingly active role in the surveillance of major global health challenges, such as the emergence of antimicrobial resistance. The post-weaning period is of critical importance for the swine industry and antimicrobials are still required when infection occurs during this period. Here, two sequencing approaches, shotgun metagenomics and metatranscriptomics, have been applied to decipher the effect of different treatments used in post-weaning diarrhea on the transcriptome and resistome of pig gut microbiome. With this objective, a metagenome-assembled genome (MAG) catalogue was generated to use as a reference database for transcript mapping obtained from a total of 140 pig fecal samples in a cross-sectional and longitudinal design to study differential gene expression. The different treatments included antimicrobials trimethoprim/sulfamethoxazole, colistin, gentamicin, and amoxicillin, and an oral commercial vaccine, a control with water acidification, and an untreated control. For metatranscriptomics, fecal samples from pigs were selected before weaning, three days and four weeks post-treatment. Results The final non-redundant MAGs collection comprised a total of 1396 genomes obtained from single assemblies and co-assemblies per treatment group and sampling time from the metagenomics data. Analysis of antimicrobial resistance genes (ARGs) at this assembly level considerably reduced the total number of ARGs identified in comparison to those found at the reads level. Besides, from the metatranscriptomics data, half of those ARGs were detected transcriptionally active in all treatment groups. Differential gene expression between sampling times after treatment found major number of differential expressed genes (DEGs) against the group treated continuously with amoxicillin, with DEGs being correlated with antimicrobial resistance. Moreover, at three days post-treatment, a high number of significantly downregulated genes was detected in the group treated with gentamicin. At this sampling time, this group showed an altered expression of ribosomal-related genes, demonstrating the rapid effect of gentamicin to inhibit bacterial protein synthesis. Conclusions Different antimicrobial treatments can impact differently the transcriptome and resistome of microbial communities, highlighting the relevance of novel sequencing approaches to monitor the resistome and contribute to a more efficient antimicrobial stewardship.This study was funded by the I + D + I National Program RTI2018-095586-B-C22 and the CERCA program. J.G.M. is a PhD student from the Autonomous University of Barcelona, Biotechnology Program, with an IRTA fellowship from the strategic initiative on antimicrobial reduction in animal production and performed part of the analysis at the Norwegian University of Life Sciences (NMBU) with an EMBO Scientific Exchange Grant (10385). Y.R.C. is recipient of a Ramon y Cajal postdoctoral fellowship (RYC2019-027244-I) from the Spanish Ministry of Science and Innovation.info:eu-repo/semantics/publishedVersionBioMed CentralProducció AnimalSanitat AnimalGenètica i Millora Animal202520252025info:eu-repo/semantics/article16application/pdfhttp://hdl.handle.net/20.500.12327/4689https://doi.org/10.1186/s42523-025-00418-8reponame:IRTA Pubpro. Open Digital Archiveinstname:Institut de Recerca i Tecnologia Agroalimentàries (IRTA)InglésAnimal MicrobiomeMICIU/Programa Estatal de I+D+I orientada a los retos de la sociedad/RTI2018-095586-B-C22/ES/OPTIMIZATION OF DIAGNOSIS AND TREATMENT OF POSTWEANING DIARRHEAS IN PIGS: TOWARDS A RATIONAL USE OF ANTIBIOTICS/MICIU/Programa Estatal de promoción del talento y su empleabilidad en I+D+I/RYC2019-027244-I/ES/Metagenomics and integrative biology tools to improve sustainable livestock systems/Attribution-NonCommercial-NoDerivatives 4.0 Internationalhttp://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:repositori.irta.cat:20.500.12327/46892026-06-16T08:51:17Z
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