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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...

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Autores principales: Bian, Shengzhe, Zeng, Wenhong, Li, Qiwen, Li, Yinghui, Wong, Nai-Kei, Jiang, Min, Zuo, Le, Hu, Qinghua, Li, Liqiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
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.
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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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