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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Published in | Frontiers in microbiology Vol. 11; p. 546150 |
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Main Authors | , , , , , , , , |
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Language | English |
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11.01.2021
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Abstract | 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. |
---|---|
AbstractList | 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.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. 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. 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. 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, 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 , 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 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 strains. We found a distinct pattern of CPS gene cluster across different K-serogroups and expanded its new 3'-border by identifying 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 species, gene duplication is likely to play instrumental roles in the evolution of CPS in This is the first time, to the best of our knowledge, that a large scale of CPS gene clusters of different K-serogroups in have been identified and characterized in evolutionary contexts. This work should help advance understanding on the variation of CPS in and provide a framework for developing diagnostically relevant serotyping methods. |
Author | Li, Yinghui Wong, Nai-Kei Li, Qiwen Bian, Shengzhe Jiang, Min Zuo, Le Li, Liqiang Hu, Qinghua Zeng, Wenhong |
AuthorAffiliation | 3 Shenzhen Key Laboratory of Unknown Pathogen Identification , Shenzhen , China 1 BGI Education Center, University of Chinese Academy of Sciences , Shenzhen , China 2 BGI-Shenzhen , Shenzhen , China 4 Jiangxi University of Traditional Chinese Medicine , Nanchang , China 5 Shenzhen Center for Disease Control and Prevention , Shenzhen , China 6 National Clinical Research Center for Infectious Diseases, Shenzhen Third People’s Hospital, The Second Hospital Affiliated to Southern University of Science and Technology , Shenzhen , China 7 School of Public Health (Shenzhen), Sun Yat-sen University , Guangzhou , China |
AuthorAffiliation_xml | – name: 1 BGI Education Center, University of Chinese Academy of Sciences , Shenzhen , China – name: 7 School of Public Health (Shenzhen), Sun Yat-sen University , Guangzhou , China – name: 2 BGI-Shenzhen , Shenzhen , China – name: 3 Shenzhen Key Laboratory of Unknown Pathogen Identification , Shenzhen , China – name: 4 Jiangxi University of Traditional Chinese Medicine , Nanchang , China – name: 5 Shenzhen Center for Disease Control and Prevention , Shenzhen , China – name: 6 National Clinical Research Center for Infectious Diseases, Shenzhen Third People’s Hospital, The Second Hospital Affiliated to Southern University of Science and Technology , Shenzhen , China |
Author_xml | – sequence: 1 givenname: Shengzhe surname: Bian fullname: Bian, Shengzhe – sequence: 2 givenname: Wenhong surname: Zeng fullname: Zeng, Wenhong – sequence: 3 givenname: Qiwen surname: Li fullname: Li, Qiwen – sequence: 4 givenname: Yinghui surname: Li fullname: Li, Yinghui – sequence: 5 givenname: Nai-Kei surname: Wong fullname: Wong, Nai-Kei – sequence: 6 givenname: Min surname: Jiang fullname: Jiang, Min – sequence: 7 givenname: Le surname: Zuo fullname: Zuo, Le – sequence: 8 givenname: Qinghua surname: Hu fullname: Hu, Qinghua – sequence: 9 givenname: Liqiang surname: Li fullname: Li, Liqiang |
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ContentType | Journal Article |
Copyright | Copyright © 2021 Bian, Zeng, Li, Li, Wong, Jiang, Zuo, Hu and Li. Copyright © 2021 Bian, Zeng, Li, Li, Wong, Jiang, Zuo, Hu and Li. 2021 Bian, Zeng, Li, Li, Wong, Jiang, Zuo, Hu and Li |
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Keywords | genetic structure capsule biosynthesis loci K antigen serotype Vibiro parahaemolyticus |
Language | English |
License | Copyright © 2021 Bian, Zeng, Li, Li, Wong, Jiang, Zuo, Hu and Li. 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. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Baolei Jia, Chung-Ang University, South Korea Reviewed by: Aoife Boyd, National University of Ireland Galway, Ireland; Santiago Castillo Ramírez, National Autonomous University of Mexico, Mexico These authors have contributed equally to this work This article was submitted to Evolutionary and Genomic Microbiology, a section of the journal Frontiers in Microbiology |
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Title | Genetic Structure, Function, and Evolution of Capsule Biosynthesis Loci in Vibrio parahaemolyticus |
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