Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome

Bacterial relatedness measured using select chromosomal loci forms the basis of public health genomic surveillance. While approximating vertical evolution through this approach has proven exceptionally valuable for understanding pathogen dynamics, it excludes a fundamental dimension of bacterial evo...

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Autores: Peñil-Celis, Arancha, Tagg, Kaitlin A., Webb, Hattie E., Redondo, Santiago, Watkins, Louise Francois, Vielva, Luis, Griffin, Chelsey, Kim, Justin Y., Folster, Jason P., Garcillán-Barcia, M. Pilar, Cruz, Fernando de la
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2024
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/382558
Acceso en línea:http://hdl.handle.net/10261/382558
Access Level:acceso abierto
Palabra clave:Salmonella Typhi
Pangenome
Plasmids
Antimicrobial resistance
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spelling Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenomePeñil-Celis, AranchaTagg, Kaitlin A.Webb, Hattie E.Redondo, SantiagoWatkins, Louise FrancoisVielva, LuisGriffin, ChelseyKim, Justin Y.Folster, Jason P.Garcillán-Barcia, M. PilarCruz, Fernando de laSalmonella TyphiPangenomePlasmidsAntimicrobial resistanceBacterial relatedness measured using select chromosomal loci forms the basis of public health genomic surveillance. While approximating vertical evolution through this approach has proven exceptionally valuable for understanding pathogen dynamics, it excludes a fundamental dimension of bacterial evolution—horizontal gene transfer. Incorporating the accessory genome is the logical remediation and has recently shown promise in expanding epidemiological resolution for enteric pathogens. Employing k-mer-based Jaccard index analysis, and a novel genome length distance metric, we computed pangenome (i.e., core and accessory) relatedness for the globally important pathogen Salmonella enterica serotype Typhi (Typhi), and graphically express both vertical (homology-by-descent) and horizontal (homology-by-admixture) evolutionary relationships in a reticulate network of over 2,200 U.S. Typhi genomes. This analysis revealed non-random structure in the Typhi pangenome that is driven predominantly by the gain and loss of mobile genetic elements, confirming and expanding upon known epidemiological patterns, revealing novel plasmid dynamics, and identifying avenues for further genomic epidemiological exploration. With an eye to public health application, this work adds important biological context to the rapidly improving ways of analyzing bacterial genetic data and demonstrates the value of the accessory genome to infer pathogen epidemiology and evolution.This work was supported by the Centers for Disease Control and Prevention (contract no. 75D30119C06679 and 75D30121C11978 to F.D.L.C). This work was also supported by the Spanish Ministry of Science and Innovation MCIN/AEI/10.13039/501100011033 (PID2020-117923GB-I00 to F.D.L.C. and M.P.G.-B.), and the Spanish Ministry of Economy, Industry and Competitiveness (DI-17-09164 to S.R.-S.).Peer reviewedAmerican Society for MicrobiologyCenters for Disease Control and Prevention (US)Agencia Estatal de Investigación (España)Ministerio de Ciencia, Innovación y Universidades (España)Ministerio de Economía, Industria y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252024info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/382558reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-117923GB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1128/msystems.00365-24https://doi.org/10.1128/msystems.00365-24Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3825582026-05-22T06:33:51Z
dc.title.none.fl_str_mv Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
title Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
spellingShingle Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
Peñil-Celis, Arancha
Salmonella Typhi
Pangenome
Plasmids
Antimicrobial resistance
title_short Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
title_full Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
title_fullStr Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
title_full_unstemmed Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
title_sort Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome
dc.creator.none.fl_str_mv Peñil-Celis, Arancha
Tagg, Kaitlin A.
Webb, Hattie E.
Redondo, Santiago
Watkins, Louise Francois
Vielva, Luis
Griffin, Chelsey
Kim, Justin Y.
Folster, Jason P.
Garcillán-Barcia, M. Pilar
Cruz, Fernando de la
author Peñil-Celis, Arancha
author_facet Peñil-Celis, Arancha
Tagg, Kaitlin A.
Webb, Hattie E.
Redondo, Santiago
Watkins, Louise Francois
Vielva, Luis
Griffin, Chelsey
Kim, Justin Y.
Folster, Jason P.
Garcillán-Barcia, M. Pilar
Cruz, Fernando de la
author_role author
author2 Tagg, Kaitlin A.
Webb, Hattie E.
Redondo, Santiago
Watkins, Louise Francois
Vielva, Luis
Griffin, Chelsey
Kim, Justin Y.
Folster, Jason P.
Garcillán-Barcia, M. Pilar
Cruz, Fernando de la
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Centers for Disease Control and Prevention (US)
Agencia Estatal de Investigación (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Ministerio de Economía, Industria y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Salmonella Typhi
Pangenome
Plasmids
Antimicrobial resistance
topic Salmonella Typhi
Pangenome
Plasmids
Antimicrobial resistance
description Bacterial relatedness measured using select chromosomal loci forms the basis of public health genomic surveillance. While approximating vertical evolution through this approach has proven exceptionally valuable for understanding pathogen dynamics, it excludes a fundamental dimension of bacterial evolution—horizontal gene transfer. Incorporating the accessory genome is the logical remediation and has recently shown promise in expanding epidemiological resolution for enteric pathogens. Employing k-mer-based Jaccard index analysis, and a novel genome length distance metric, we computed pangenome (i.e., core and accessory) relatedness for the globally important pathogen Salmonella enterica serotype Typhi (Typhi), and graphically express both vertical (homology-by-descent) and horizontal (homology-by-admixture) evolutionary relationships in a reticulate network of over 2,200 U.S. Typhi genomes. This analysis revealed non-random structure in the Typhi pangenome that is driven predominantly by the gain and loss of mobile genetic elements, confirming and expanding upon known epidemiological patterns, revealing novel plasmid dynamics, and identifying avenues for further genomic epidemiological exploration. With an eye to public health application, this work adds important biological context to the rapidly improving ways of analyzing bacterial genetic data and demonstrates the value of the accessory genome to infer pathogen epidemiology and evolution.
publishDate 2024
dc.date.none.fl_str_mv 2024
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/382558
url http://hdl.handle.net/10261/382558
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2020-117923GB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1128/msystems.00365-24
https://doi.org/10.1128/msystems.00365-24
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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