Genetic structure, function and evolution of capsule biosynthesis loci inVibrio parahaemolyticus
Authors: Bian Shengzhe , Wenhong Zeng , Li Qiwen , Li Yinghui , Wong Nai-Kei , Jiang Min , Zuo Le , Hu Qinghua , Li Liqiang 
Published: February 2020

Capsule-forming extracellular polysaccharides are crucial to bacterial host colonization, invasion, immune evasion and ultimately pathogenicity. Due to warming ocean waters and human encroachment of coastal ecosystems,Vibrio parahaemolyticushas emerged as a globally important food-borne 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 serotypingV. parahaemolyticus, while 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 inV. parahaemolyticuspathophysiology. 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 443V. parahaemolyticusstrains. We found a distinct pattern of CPS gene cluster across different K-serogroups, and expanded its new right-border by identifyingglpXas a key gene conserved across all serotypes. 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 otherVibriospecies, gene duplication and nonsense mutations are likely to play instrumental roles in the evolution of CPS inV. parahaemolyticus.It is the first time, to the best of our knowledge, that a large-scale of CPS gene clusters of different K-serogroups inV. parahaemolyticushave been identified and characterized in evolutionary contexts. This work should help advance understanding on the variation of CPS inV. parahaemolyticus, and provide a framework for developing diagnostically relevant serotyping methods.

Author summary

Due to warming ocean waters and human encroachment of coastal ecosystems,Vibrio parahaemolyticushas emerged as a globally important food-borne enteropathogen. However, the genetic structure of CPS loci for 71 K-serogroupsV. parahaemolyticushave remained unidentified, limiting progress in understanding its roles inV. parahaemolyticuspathophysiology. In this study, we identified and characterized the genetic structure of CPS loci of 40 K-serogroups through whole genome sequencing of 443V. parahaemolyticusstrains. We expanded and identified its new right-border by identifyingglpXas a key gene conserved across all serotypes. We proposed an evolution model of the CPS gene clusters of 40 K-serogroups. We also found horizontal gene transfer by recombination from otherVibriospecies, gene duplication and nonsense mutations are likely to play instrumental roles in the evolution of CPS inV. parahaemolyticus.It is the first time, to the best of our knowledge, that a large-scale of CPS loci of different K-serogroups inV. parahaemolyticushave been identified and characterized in evolutionary contexts. This work should help advance understanding on the variation of CPS inV. parahaemolyticus, and provide a framework for developing diagnostically relevant serotyping methods.