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Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster

Vibrio anguillarum is the most frequent pathogen affecting fish worldwide. The only known virulent strains of V. anguillarum are serotypes O1, O2, and O3. Genetic differences between the serotypes that could shed insight on the evolution and serotype differences of this marine pathogen are unknown....

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Autores principales: Machimbirike, Vimbai Irene, Vasquez, Ignacio, Cao, Trung, Chukwu-Osazuwa, Joy, Onireti, Oluwatoyin, Segovia, Cristopher, Khunrae, Pongsak, Rattanarojpong, Triwit, Booman, Marije, Jones, Simon, Soto-Davila, Manuel, Dixon, Brian, Santander, Javier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10059132/
https://www.ncbi.nlm.nih.gov/pubmed/36985365
http://dx.doi.org/10.3390/microorganisms11030792
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author Machimbirike, Vimbai Irene
Vasquez, Ignacio
Cao, Trung
Chukwu-Osazuwa, Joy
Onireti, Oluwatoyin
Segovia, Cristopher
Khunrae, Pongsak
Rattanarojpong, Triwit
Booman, Marije
Jones, Simon
Soto-Davila, Manuel
Dixon, Brian
Santander, Javier
author_facet Machimbirike, Vimbai Irene
Vasquez, Ignacio
Cao, Trung
Chukwu-Osazuwa, Joy
Onireti, Oluwatoyin
Segovia, Cristopher
Khunrae, Pongsak
Rattanarojpong, Triwit
Booman, Marije
Jones, Simon
Soto-Davila, Manuel
Dixon, Brian
Santander, Javier
author_sort Machimbirike, Vimbai Irene
collection PubMed
description Vibrio anguillarum is the most frequent pathogen affecting fish worldwide. The only known virulent strains of V. anguillarum are serotypes O1, O2, and O3. Genetic differences between the serotypes that could shed insight on the evolution and serotype differences of this marine pathogen are unknown. Here, we fully sequenced and characterized a strain of V. anguillarum O1 (J382) isolated from winter steelhead trout (Oncorhynchus mykiss irideus) in British Columbia, Canada. Koch’s postulates using the O1 strain were replicated in naïve lumpfish (Cyclopterus lumpus) and compared to O2. Phenotypic and genotypic comparisons were conducted for serotypes O1, O2, and O3, using biochemical tests and bioinformatic tools, respectively. The genome of V. anguillarum O1 (J382) contains two chromosomes (3.13 Mb and 1.03 Mb) and two typical pJM1-like plasmids (65,573 and 76,959 bp). Furthermore, V. anguillarum O1 (J382) displayed resistance to colistin sulphate, which differs from serotype O2 and could be attributed to the presence of the ugd gene. Comparative genomic analysis, among the serotypes, showed that intra-species evolution is driven by insertion sequences, bacteriophages, and a different repertoire of putative ncRNAs. Genetic heterogeneity in the O-antigen biosynthesis gene cluster is characterized by the absence or the presence of unique genes, which could result in differences in the immune evasion mechanisms employed by the respective serotypes. This study contributes to understanding the genetic differences among V. anguillarum serovars and their evolution.
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spelling pubmed-100591322023-03-30 Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster Machimbirike, Vimbai Irene Vasquez, Ignacio Cao, Trung Chukwu-Osazuwa, Joy Onireti, Oluwatoyin Segovia, Cristopher Khunrae, Pongsak Rattanarojpong, Triwit Booman, Marije Jones, Simon Soto-Davila, Manuel Dixon, Brian Santander, Javier Microorganisms Article Vibrio anguillarum is the most frequent pathogen affecting fish worldwide. The only known virulent strains of V. anguillarum are serotypes O1, O2, and O3. Genetic differences between the serotypes that could shed insight on the evolution and serotype differences of this marine pathogen are unknown. Here, we fully sequenced and characterized a strain of V. anguillarum O1 (J382) isolated from winter steelhead trout (Oncorhynchus mykiss irideus) in British Columbia, Canada. Koch’s postulates using the O1 strain were replicated in naïve lumpfish (Cyclopterus lumpus) and compared to O2. Phenotypic and genotypic comparisons were conducted for serotypes O1, O2, and O3, using biochemical tests and bioinformatic tools, respectively. The genome of V. anguillarum O1 (J382) contains two chromosomes (3.13 Mb and 1.03 Mb) and two typical pJM1-like plasmids (65,573 and 76,959 bp). Furthermore, V. anguillarum O1 (J382) displayed resistance to colistin sulphate, which differs from serotype O2 and could be attributed to the presence of the ugd gene. Comparative genomic analysis, among the serotypes, showed that intra-species evolution is driven by insertion sequences, bacteriophages, and a different repertoire of putative ncRNAs. Genetic heterogeneity in the O-antigen biosynthesis gene cluster is characterized by the absence or the presence of unique genes, which could result in differences in the immune evasion mechanisms employed by the respective serotypes. This study contributes to understanding the genetic differences among V. anguillarum serovars and their evolution. MDPI 2023-03-20 /pmc/articles/PMC10059132/ /pubmed/36985365 http://dx.doi.org/10.3390/microorganisms11030792 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Machimbirike, Vimbai Irene
Vasquez, Ignacio
Cao, Trung
Chukwu-Osazuwa, Joy
Onireti, Oluwatoyin
Segovia, Cristopher
Khunrae, Pongsak
Rattanarojpong, Triwit
Booman, Marije
Jones, Simon
Soto-Davila, Manuel
Dixon, Brian
Santander, Javier
Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
title Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
title_full Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
title_fullStr Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
title_full_unstemmed Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
title_short Comparative Genomic Analysis of Virulent Vibrio (Listonella) anguillarum Serotypes Revealed Genetic Diversity and Genomic Signatures in the O-Antigen Biosynthesis Gene Cluster
title_sort comparative genomic analysis of virulent vibrio (listonella) anguillarum serotypes revealed genetic diversity and genomic signatures in the o-antigen biosynthesis gene cluster
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10059132/
https://www.ncbi.nlm.nih.gov/pubmed/36985365
http://dx.doi.org/10.3390/microorganisms11030792
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