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

Abstract 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...

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Main Authors: Jai W. Mehat, Roberto M. La Ragione, Arnoud H. M. van Vliet
Format: Article
Language:English
Published: BMC 2020-04-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-6704-z
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spelling doaj-06ea9f335a984ad5983d16313e06261e2020-11-25T02:59:49ZengBMCBMC Genomics1471-21642020-04-0121111110.1186/s12864-020-6704-zCampylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decayJai W. Mehat0Roberto M. La Ragione1Arnoud H. M. van Vliet2Department of Pathology and Infectious Diseases, School of Veterinary Medicine, University of SurreyDepartment of Pathology and Infectious Diseases, School of Veterinary Medicine, University of SurreyDepartment of Pathology and Infectious Diseases, School of Veterinary Medicine, University of SurreyAbstract 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.http://link.springer.com/article/10.1186/s12864-020-6704-zCampylobacterJejuniColiAutotransporter proteinsGenomicsRecombination
collection DOAJ
language English
format Article
sources DOAJ
author Jai W. Mehat
Roberto M. La Ragione
Arnoud H. M. van Vliet
spellingShingle Jai W. Mehat
Roberto M. La Ragione
Arnoud H. M. van Vliet
Campylobacter jejuni and Campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
BMC Genomics
Campylobacter
Jejuni
Coli
Autotransporter proteins
Genomics
Recombination
author_facet Jai W. Mehat
Roberto M. La Ragione
Arnoud H. M. van Vliet
author_sort Jai W. Mehat
title 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_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_sort campylobacter jejuni and campylobacter coli autotransporter genes exhibit lineage-associated distribution and decay
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-04-01
description Abstract 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.
topic Campylobacter
Jejuni
Coli
Autotransporter proteins
Genomics
Recombination
url http://link.springer.com/article/10.1186/s12864-020-6704-z
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