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Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay

BACKGROUND: Campylobacter jejuni and Campylobacter coli are major global causes of bacterial gastroenteritis. Whilst several individual colonisation and virulence factors have been identified, our understanding of their role in the transmission, pathogenesis and ecology of Campylobacter has been ham...

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Autores principales: Mehat, Jai W., La Ragione, Roberto M., van Vliet, Arnoud H. M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7168839/
https://www.ncbi.nlm.nih.gov/pubmed/32306949
http://dx.doi.org/10.1186/s12864-020-6704-z
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author Mehat, Jai W.
La Ragione, Roberto M.
van Vliet, Arnoud H. M.
author_facet Mehat, Jai W.
La Ragione, Roberto M.
van Vliet, Arnoud H. M.
author_sort Mehat, Jai W.
collection PubMed
description BACKGROUND: Campylobacter jejuni and Campylobacter coli are major global causes of bacterial gastroenteritis. Whilst several individual colonisation and virulence factors have been identified, our understanding of their role in the transmission, pathogenesis and ecology of Campylobacter has been hampered by the genotypic and phenotypic diversity within C. jejuni and C. coli. Autotransporter proteins are a family of outer membrane or secreted proteins in Gram-negative bacteria such as Campylobacter, which are associated with virulence functions. In this study we have examined the distribution and predicted functionality of the previously described capC and the newly identified, related capD autotransporter gene families in Campylobacter. RESULTS: Two capC-like autotransporter families, designated capC and capD, were identified by homology searches of genomes of the genus Campylobacter. Each family contained four distinct orthologs of CapC and CapD. The distribution of these autotransporter genes was determined in 5829 C. jejuni and 1347 C. coli genomes. Autotransporter genes were found as intact, complete copies and inactive formats due to premature stop codons and frameshift mutations. Presence of inactive and intact autotransporter genes was associated with C. jejuni and C. coli multi-locus sequence types, but for capC, inactivation was independent from the length of homopolymeric tracts in the region upstream of the capC gene. Inactivation of capC or capD genes appears to represent lineage-specific gene decay of autotransporter genes. Intact capC genes were predominantly associated with the C. jejuni ST-45 and C. coli ST-828 generalist lineages. The capD3 gene was only found in the environmental C. coli Clade 3 lineage. These combined data support a scenario of inter-lineage and interspecies exchange of capC and subsets of capD autotransporters. CONCLUSIONS: In this study we have identified two novel, related autotransporter gene families in the genus Campylobacter, which are not uniformly present and exhibit lineage-specific associations and gene decay. The distribution and decay of the capC and capD genes exemplifies the erosion of species barriers between certain lineages of C. jejuni and C. coli, probably arising through co-habitation. This may have implications for the phenotypic variability of these two pathogens and provide opportunity for new, hybrid genotypes to emerge.
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spelling pubmed-71688392020-04-23 Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay Mehat, Jai W. La Ragione, Roberto M. van Vliet, Arnoud H. M. BMC Genomics Research Article BACKGROUND: Campylobacter jejuni and Campylobacter coli are major global causes of bacterial gastroenteritis. Whilst several individual colonisation and virulence factors have been identified, our understanding of their role in the transmission, pathogenesis and ecology of Campylobacter has been hampered by the genotypic and phenotypic diversity within C. jejuni and C. coli. Autotransporter proteins are a family of outer membrane or secreted proteins in Gram-negative bacteria such as Campylobacter, which are associated with virulence functions. In this study we have examined the distribution and predicted functionality of the previously described capC and the newly identified, related capD autotransporter gene families in Campylobacter. RESULTS: Two capC-like autotransporter families, designated capC and capD, were identified by homology searches of genomes of the genus Campylobacter. Each family contained four distinct orthologs of CapC and CapD. The distribution of these autotransporter genes was determined in 5829 C. jejuni and 1347 C. coli genomes. Autotransporter genes were found as intact, complete copies and inactive formats due to premature stop codons and frameshift mutations. Presence of inactive and intact autotransporter genes was associated with C. jejuni and C. coli multi-locus sequence types, but for capC, inactivation was independent from the length of homopolymeric tracts in the region upstream of the capC gene. Inactivation of capC or capD genes appears to represent lineage-specific gene decay of autotransporter genes. Intact capC genes were predominantly associated with the C. jejuni ST-45 and C. coli ST-828 generalist lineages. The capD3 gene was only found in the environmental C. coli Clade 3 lineage. These combined data support a scenario of inter-lineage and interspecies exchange of capC and subsets of capD autotransporters. CONCLUSIONS: In this study we have identified two novel, related autotransporter gene families in the genus Campylobacter, which are not uniformly present and exhibit lineage-specific associations and gene decay. The distribution and decay of the capC and capD genes exemplifies the erosion of species barriers between certain lineages of C. jejuni and C. coli, probably arising through co-habitation. This may have implications for the phenotypic variability of these two pathogens and provide opportunity for new, hybrid genotypes to emerge. BioMed Central 2020-04-19 /pmc/articles/PMC7168839/ /pubmed/32306949 http://dx.doi.org/10.1186/s12864-020-6704-z Text en © The Author(s). 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Mehat, Jai W.
La Ragione, Roberto M.
van Vliet, Arnoud H. M.
Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
title Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
title_full Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
title_fullStr Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
title_full_unstemmed Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
title_short Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
title_sort campylobacter jejuni and campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7168839/
https://www.ncbi.nlm.nih.gov/pubmed/32306949
http://dx.doi.org/10.1186/s12864-020-6704-z
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