Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies

ABSTRACT Salmonella is responsible for many nontyphoidal foodborne infections and enteric (typhoid) fever in humans. Of the two Salmonella species, Salmonella enterica is highly diverse and includes 10 known subspecies and approximately 2,600 serotypes. Understanding the evolutionary processes that...

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Autores principales:	Cooper J. Park, Cheryl P. Andam
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Salmonella genome pan-genome recombination subspecies Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7e4d24a44022479bb1184e01ed981ab9
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spelling	oai:doaj.org-article:7e4d24a44022479bb1184e01ed981ab92021-12-02T19:47:38ZDistinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies10.1128/mSystems.00515-192379-5077https://doaj.org/article/7e4d24a44022479bb1184e01ed981ab92020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00515-19https://doaj.org/toc/2379-5077ABSTRACT Salmonella is responsible for many nontyphoidal foodborne infections and enteric (typhoid) fever in humans. Of the two Salmonella species, Salmonella enterica is highly diverse and includes 10 known subspecies and approximately 2,600 serotypes. Understanding the evolutionary processes that generate the tremendous diversity in Salmonella is important in reducing and controlling the incidence of disease outbreaks and the emergence of virulent strains. In this study, we aim to elucidate the impact of homologous recombination in the diversification of S. enterica subspecies. Using a data set of previously published 926 Salmonella genomes representing the 10 S. enterica subspecies and Salmonella bongori, we calculated a genus-wide pan-genome composed of 84,041 genes and the S. enterica pan-genome of 81,371 genes. The size of the accessory genomes varies between 12,429 genes in S. enterica subsp. arizonae (subsp. IIIa) to 33,257 genes in S. enterica subsp. enterica (subsp. I). A total of 12,136 genes in the Salmonella pan-genome show evidence of recombination, representing 14.44% of the pan-genome. We identified genomic hot spots of recombination that include genes associated with flagellin and the synthesis of methionine and thiamine pyrophosphate, which are known to influence host adaptation and virulence. Last, we uncovered within-species heterogeneity in rates of recombination and preferential genetic exchange between certain donor and recipient strains. Frequent but biased recombination within a bacterial species may suggest that lineages vary in their response to environmental selection pressure. Certain lineages, such as the more uncommon non-enterica subspecies (non-S. enterica subsp. enterica), may also act as a major reservoir of genetic diversity for the wider population. IMPORTANCE S. enterica is a major foodborne pathogen, which can be transmitted via several distinct routes from animals and environmental sources to human hosts. Multiple subspecies and serotypes of S. enterica exhibit considerable differences in virulence, host specificity, and colonization. This study provides detailed insights into the dynamics of recombination and its contributions to S. enterica subspecies evolution. Widespread recombination within the species means that new adaptations arising in one lineage can be rapidly transferred to another lineage. We therefore predict that recombination has been an important factor in the emergence of several major disease-causing strains from diverse genomic backgrounds and their ability to adapt to disparate environments.Cooper J. ParkCheryl P. AndamAmerican Society for MicrobiologyarticleSalmonellagenomepan-genomerecombinationsubspeciesMicrobiologyQR1-502ENmSystems, Vol 5, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Salmonella genome pan-genome recombination subspecies Microbiology QR1-502
spellingShingle	Salmonella genome pan-genome recombination subspecies Microbiology QR1-502 Cooper J. Park Cheryl P. Andam Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies
description	ABSTRACT Salmonella is responsible for many nontyphoidal foodborne infections and enteric (typhoid) fever in humans. Of the two Salmonella species, Salmonella enterica is highly diverse and includes 10 known subspecies and approximately 2,600 serotypes. Understanding the evolutionary processes that generate the tremendous diversity in Salmonella is important in reducing and controlling the incidence of disease outbreaks and the emergence of virulent strains. In this study, we aim to elucidate the impact of homologous recombination in the diversification of S. enterica subspecies. Using a data set of previously published 926 Salmonella genomes representing the 10 S. enterica subspecies and Salmonella bongori, we calculated a genus-wide pan-genome composed of 84,041 genes and the S. enterica pan-genome of 81,371 genes. The size of the accessory genomes varies between 12,429 genes in S. enterica subsp. arizonae (subsp. IIIa) to 33,257 genes in S. enterica subsp. enterica (subsp. I). A total of 12,136 genes in the Salmonella pan-genome show evidence of recombination, representing 14.44% of the pan-genome. We identified genomic hot spots of recombination that include genes associated with flagellin and the synthesis of methionine and thiamine pyrophosphate, which are known to influence host adaptation and virulence. Last, we uncovered within-species heterogeneity in rates of recombination and preferential genetic exchange between certain donor and recipient strains. Frequent but biased recombination within a bacterial species may suggest that lineages vary in their response to environmental selection pressure. Certain lineages, such as the more uncommon non-enterica subspecies (non-S. enterica subsp. enterica), may also act as a major reservoir of genetic diversity for the wider population. IMPORTANCE S. enterica is a major foodborne pathogen, which can be transmitted via several distinct routes from animals and environmental sources to human hosts. Multiple subspecies and serotypes of S. enterica exhibit considerable differences in virulence, host specificity, and colonization. This study provides detailed insights into the dynamics of recombination and its contributions to S. enterica subspecies evolution. Widespread recombination within the species means that new adaptations arising in one lineage can be rapidly transferred to another lineage. We therefore predict that recombination has been an important factor in the emergence of several major disease-causing strains from diverse genomic backgrounds and their ability to adapt to disparate environments.
format	article
author	Cooper J. Park Cheryl P. Andam
author_facet	Cooper J. Park Cheryl P. Andam
author_sort	Cooper J. Park
title	Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies
title_short	Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies
title_full	Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies
title_fullStr	Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies
title_full_unstemmed	Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies
title_sort	distinct but intertwined evolutionary histories of multiple <named-content content-type="genus-species">salmonella enterica</named-content> subspecies
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/7e4d24a44022479bb1184e01ed981ab9
work_keys_str_mv	AT cooperjpark distinctbutintertwinedevolutionaryhistoriesofmultiplenamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentsubspecies AT cherylpandam distinctbutintertwinedevolutionaryhistoriesofmultiplenamedcontentcontenttypegenusspeciessalmonellaentericanamedcontentsubspecies
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Distinct but Intertwined Evolutionary Histories of Multiple <named-content content-type="genus-species">Salmonella enterica</named-content> Subspecies

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