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Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus
Capsule-forming extracellular polysaccharides are crucial for bacterial host colonization, invasion, immune evasion, and ultimately pathogenicity. Due to warming ocean waters and human encroachment of coastal ecosystems, Vibrio parahaemolyticus has emerged as a globally important foodborne enteropat...
Autores principales: | , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7829505/ https://www.ncbi.nlm.nih.gov/pubmed/33505361 http://dx.doi.org/10.3389/fmicb.2020.546150 |
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author | Bian, Shengzhe Zeng, Wenhong Li, Qiwen Li, Yinghui Wong, Nai-Kei Jiang, Min Zuo, Le Hu, Qinghua Li, Liqiang |
author_facet | Bian, Shengzhe Zeng, Wenhong Li, Qiwen Li, Yinghui Wong, Nai-Kei Jiang, Min Zuo, Le Hu, Qinghua Li, Liqiang |
author_sort | Bian, Shengzhe |
collection | PubMed |
description | Capsule-forming extracellular polysaccharides are crucial for bacterial host colonization, invasion, immune evasion, and ultimately pathogenicity. Due to warming ocean waters and human encroachment of coastal ecosystems, Vibrio parahaemolyticus has emerged as a globally important foodborne enteropathogen implicated in acute gastroenteritis, wound infections, and septic shock. Conventionally, the antigenic properties of lipopolysaccharide (LPS, O antigen) and capsular polysaccharide (CPS, K antigen) have provided a basis for serotyping V. parahaemolyticus, whereas disclosure of genetic elements encoding 13 O-serogroups have allowed molecular serotyping methods to be developed. However, the genetic structure of CPS loci for 71 K-serogroups has remained unidentified, limiting progress in understanding its roles in V. parahaemolyticus pathophysiology. In this study, we identified and characterized the genetic structure and their evolutionary relationship of CPS loci of 40 K-serogroups through whole genome sequencing of 443 V. parahaemolyticus strains. We found a distinct pattern of CPS gene cluster across different K-serogroups and expanded its new 3′-border by identifying glpX as a key gene conserved across all K-serogroups. A total of 217 genes involved in CPS biosynthesis were annotated. Functional contents and genetic structure of the 40 K-serogroups were analyzed. Based on inferences from species trees and gene trees, we proposed an evolution model of the CPS gene clusters of 40 K-serogroups. Horizontal gene transfer by recombination from other Vibrio species, gene duplication is likely to play instrumental roles in the evolution of CPS in V. parahaemolyticus. This is the first time, to the best of our knowledge, that a large scale of CPS gene clusters of different K-serogroups in V. parahaemolyticus have been identified and characterized in evolutionary contexts. This work should help advance understanding on the variation of CPS in V. parahaemolyticus and provide a framework for developing diagnostically relevant serotyping methods. |
format | Online Article Text |
id | pubmed-7829505 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-78295052021-01-26 Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus Bian, Shengzhe Zeng, Wenhong Li, Qiwen Li, Yinghui Wong, Nai-Kei Jiang, Min Zuo, Le Hu, Qinghua Li, Liqiang Front Microbiol Microbiology Capsule-forming extracellular polysaccharides are crucial for bacterial host colonization, invasion, immune evasion, and ultimately pathogenicity. Due to warming ocean waters and human encroachment of coastal ecosystems, Vibrio parahaemolyticus has emerged as a globally important foodborne enteropathogen implicated in acute gastroenteritis, wound infections, and septic shock. Conventionally, the antigenic properties of lipopolysaccharide (LPS, O antigen) and capsular polysaccharide (CPS, K antigen) have provided a basis for serotyping V. parahaemolyticus, whereas disclosure of genetic elements encoding 13 O-serogroups have allowed molecular serotyping methods to be developed. However, the genetic structure of CPS loci for 71 K-serogroups has remained unidentified, limiting progress in understanding its roles in V. parahaemolyticus pathophysiology. In this study, we identified and characterized the genetic structure and their evolutionary relationship of CPS loci of 40 K-serogroups through whole genome sequencing of 443 V. parahaemolyticus strains. We found a distinct pattern of CPS gene cluster across different K-serogroups and expanded its new 3′-border by identifying glpX as a key gene conserved across all K-serogroups. A total of 217 genes involved in CPS biosynthesis were annotated. Functional contents and genetic structure of the 40 K-serogroups were analyzed. Based on inferences from species trees and gene trees, we proposed an evolution model of the CPS gene clusters of 40 K-serogroups. Horizontal gene transfer by recombination from other Vibrio species, gene duplication is likely to play instrumental roles in the evolution of CPS in V. parahaemolyticus. This is the first time, to the best of our knowledge, that a large scale of CPS gene clusters of different K-serogroups in V. parahaemolyticus have been identified and characterized in evolutionary contexts. This work should help advance understanding on the variation of CPS in V. parahaemolyticus and provide a framework for developing diagnostically relevant serotyping methods. Frontiers Media S.A. 2021-01-11 /pmc/articles/PMC7829505/ /pubmed/33505361 http://dx.doi.org/10.3389/fmicb.2020.546150 Text en Copyright © 2021 Bian, Zeng, Li, Li, Wong, Jiang, Zuo, Hu and Li. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Bian, Shengzhe Zeng, Wenhong Li, Qiwen Li, Yinghui Wong, Nai-Kei Jiang, Min Zuo, Le Hu, Qinghua Li, Liqiang Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
title | Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
title_full | Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
title_fullStr | Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
title_full_unstemmed | Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
title_short | Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
title_sort | genetic structure, function, and evolution of capsule biosynthesis loci in vibrio parahaemolyticus |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7829505/ https://www.ncbi.nlm.nih.gov/pubmed/33505361 http://dx.doi.org/10.3389/fmicb.2020.546150 |
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