Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution

Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution

Bacteria of the genus Salmonella comprise a large and evolutionary related population of zoonotic pathogens that can infect mammals, including humans and domestic animals, birds, reptiles and amphibians. Salmonella carries a plethora of virulence genes, including fimbrial adhesins, some of them know...

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Main Authors: Yue, Min, Rankin, Shelley C., Blanchet, Ryan T., Nulton, James D., Edwards, Robert A., Schifferli, Dieter M.
Format: Online
Language:English
Published: Public Library of Science 2012
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3373541/
id pubmed-3373541
recordtype oai_dc
spelling pubmed-33735412012-06-14 Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution Yue, Min Rankin, Shelley C. Blanchet, Ryan T. Nulton, James D. Edwards, Robert A. Schifferli, Dieter M. Research Article Bacteria of the genus Salmonella comprise a large and evolutionary related population of zoonotic pathogens that can infect mammals, including humans and domestic animals, birds, reptiles and amphibians. Salmonella carries a plethora of virulence genes, including fimbrial adhesins, some of them known to participate in mammalian or avian host colonization. Each type of fimbria has its structural subunit and biogenesis genes encoded by one fimbrial gene cluster (FGC). The accumulation of new genomic information offered a timely opportunity to better evaluate the number and types of FGCs in the Salmonella pangenome, to test the use of current classifications based on phylogeny, and to infer potential correlations between FGC evolution in various Salmonella serovars and host niches. This study focused on the FGCs of the currently deciphered 90 genomes and 60 plasmids of Salmonella. The analysis highlighted a fimbriome consisting of 35 different FGCs, of which 16 were new, each strain carrying between 5 and 14 FGCs. The Salmonella fimbriome was extremely diverse with FGC representatives in 8 out of 9 previously categorized fimbrial clades and subclades. Phylogenetic analysis of Salmonella suggested macroevolutionary shifts detectable by extensive FGC deletion and acquisition. In addition, microevolutionary drifts were best depicted by the high level of allelic variation in predicted or known adhesins, such as the type 1 fimbrial adhesin FimH for which 67 different natural alleles were identified in S. enterica subsp. I. Together with strain-specific collections of FGCs, allelic variation among adhesins attested to the pathoadaptive evolution of Salmonella towards specific hosts and tissues, potentially modulating host range, strain virulence, disease progression, and transmission efficiency. Further understanding of how each Salmonella strain utilizes its panel of FGCs and specific adhesin alleles for survival and infection will support the development of new approaches for the control of Salmonellosis. Public Library of Science 2012-06-12 /pmc/articles/PMC3373541/ /pubmed/22701679 http://dx.doi.org/10.1371/journal.pone.0038596 Text en Yue et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Yue, Min
Rankin, Shelley C.
Blanchet, Ryan T.
Nulton, James D.
Edwards, Robert A.
Schifferli, Dieter M.
spellingShingle Yue, Min
Rankin, Shelley C.
Blanchet, Ryan T.
Nulton, James D.
Edwards, Robert A.
Schifferli, Dieter M.
Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
author_facet Yue, Min
Rankin, Shelley C.
Blanchet, Ryan T.
Nulton, James D.
Edwards, Robert A.
Schifferli, Dieter M.
author_sort Yue, Min
title Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
title_short Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
title_full Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
title_fullStr Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
title_full_unstemmed Diversification of the Salmonella Fimbriae: A Model of Macro- and Microevolution
title_sort diversification of the salmonella fimbriae: a model of macro- and microevolution
description Bacteria of the genus Salmonella comprise a large and evolutionary related population of zoonotic pathogens that can infect mammals, including humans and domestic animals, birds, reptiles and amphibians. Salmonella carries a plethora of virulence genes, including fimbrial adhesins, some of them known to participate in mammalian or avian host colonization. Each type of fimbria has its structural subunit and biogenesis genes encoded by one fimbrial gene cluster (FGC). The accumulation of new genomic information offered a timely opportunity to better evaluate the number and types of FGCs in the Salmonella pangenome, to test the use of current classifications based on phylogeny, and to infer potential correlations between FGC evolution in various Salmonella serovars and host niches. This study focused on the FGCs of the currently deciphered 90 genomes and 60 plasmids of Salmonella. The analysis highlighted a fimbriome consisting of 35 different FGCs, of which 16 were new, each strain carrying between 5 and 14 FGCs. The Salmonella fimbriome was extremely diverse with FGC representatives in 8 out of 9 previously categorized fimbrial clades and subclades. Phylogenetic analysis of Salmonella suggested macroevolutionary shifts detectable by extensive FGC deletion and acquisition. In addition, microevolutionary drifts were best depicted by the high level of allelic variation in predicted or known adhesins, such as the type 1 fimbrial adhesin FimH for which 67 different natural alleles were identified in S. enterica subsp. I. Together with strain-specific collections of FGCs, allelic variation among adhesins attested to the pathoadaptive evolution of Salmonella towards specific hosts and tissues, potentially modulating host range, strain virulence, disease progression, and transmission efficiency. Further understanding of how each Salmonella strain utilizes its panel of FGCs and specific adhesin alleles for survival and infection will support the development of new approaches for the control of Salmonellosis.
publisher Public Library of Science
publishDate 2012
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3373541/
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