Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype

ABSTRACT Vibrio vulnificus, an opportunistic pathogen, is the causative agent of a life-threatening septicemia and a rising problem for aquaculture worldwide. The genetic factors that differentiate its clinical and environmental strains remain enigmatic. Furthermore, clinical strains have emerged fr...

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Autores principales:	Mario López-Pérez, Jane M. Jayakumar, Jose M. Haro-Moreno, Asier Zaragoza-Solas, Geethika Reddi, Francisco Rodriguez-Valera, Orr H. Shapiro, Munirul Alam, Salvador Almagro-Moreno
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Vibrio vulnificus emergence evolution genomics waterborne pathogens Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ba6067968c0c4b88b0a62c36491eb4bb
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spelling	oai:doaj.org-article:ba6067968c0c4b88b0a62c36491eb4bb2021-11-15T15:55:14ZEvolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype10.1128/mBio.02852-182150-7511https://doaj.org/article/ba6067968c0c4b88b0a62c36491eb4bb2019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02852-18https://doaj.org/toc/2150-7511ABSTRACT Vibrio vulnificus, an opportunistic pathogen, is the causative agent of a life-threatening septicemia and a rising problem for aquaculture worldwide. The genetic factors that differentiate its clinical and environmental strains remain enigmatic. Furthermore, clinical strains have emerged from every clade of V. vulnificus. In this work, we investigated the underlying genomic properties and population dynamics of the V. vulnificus species from an evolutionary and ecological point of view. Genome comparisons and bioinformatic analyses of 113 V. vulnificus isolates indicate that the population of V. vulnificus is made up of four different clusters. We found evidence that recombination and gene flow between the two largest clusters (cluster 1 [C1] and C2) have drastically decreased to the point where they are diverging independently. Pangenome and phenotypic analyses showed two markedly different lifestyles for these two clusters, indicating commensal (C2) and bloomer (C1) ecotypes, with differences in carbohydrate utilization, defense systems, and chemotaxis, among other characteristics. Nonetheless, we identified frequent intra- and interspecies exchange of mobile genetic elements (e.g., antibiotic resistance plasmids, novel “chromids,” or two different and concurrent type VI secretion systems) that provide high levels of genetic diversity in the population. Surprisingly, we identified strains from both clusters in the mucosa of aquaculture species, indicating that manmade niches are bringing strains from the two clusters together. We propose an evolutionary model of V. vulnificus that could be broadly applicable to other pathogenic vibrios and facultative bacterial pathogens to pursue strategies to prevent their infections and emergence. IMPORTANCE Vibrio vulnificus is an emergent marine pathogen and is the cause of a deadly septicemia. However, the genetic factors that differentiate its clinical and environmental strains and its several biotypes remain mostly enigmatic. In this work, we investigated the underlying genomic properties and population dynamics of the V. vulnificus species to elucidate the traits that make these strains emerge as a human pathogen. The acquisition of different ecological determinants could have allowed the development of highly divergent clusters with different lifestyles within the same environment. However, we identified strains from both clusters in the mucosa of aquaculture species, indicating that manmade niches are bringing strains from the two clusters together, posing a potential risk of recombination and of emergence of novel variants. We propose a new evolutionary model that provides a perspective that could be broadly applicable to other pathogenic vibrios and facultative bacterial pathogens to pursue strategies to prevent their infections.Mario López-PérezJane M. JayakumarJose M. Haro-MorenoAsier Zaragoza-SolasGeethika ReddiFrancisco Rodriguez-ValeraOrr H. ShapiroMunirul AlamSalvador Almagro-MorenoAmerican Society for MicrobiologyarticleVibrio vulnificusemergenceevolutiongenomicswaterborne pathogensMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Vibrio vulnificus emergence evolution genomics waterborne pathogens Microbiology QR1-502
spellingShingle	Vibrio vulnificus emergence evolution genomics waterborne pathogens Microbiology QR1-502 Mario López-Pérez Jane M. Jayakumar Jose M. Haro-Moreno Asier Zaragoza-Solas Geethika Reddi Francisco Rodriguez-Valera Orr H. Shapiro Munirul Alam Salvador Almagro-Moreno Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype
description	ABSTRACT Vibrio vulnificus, an opportunistic pathogen, is the causative agent of a life-threatening septicemia and a rising problem for aquaculture worldwide. The genetic factors that differentiate its clinical and environmental strains remain enigmatic. Furthermore, clinical strains have emerged from every clade of V. vulnificus. In this work, we investigated the underlying genomic properties and population dynamics of the V. vulnificus species from an evolutionary and ecological point of view. Genome comparisons and bioinformatic analyses of 113 V. vulnificus isolates indicate that the population of V. vulnificus is made up of four different clusters. We found evidence that recombination and gene flow between the two largest clusters (cluster 1 [C1] and C2) have drastically decreased to the point where they are diverging independently. Pangenome and phenotypic analyses showed two markedly different lifestyles for these two clusters, indicating commensal (C2) and bloomer (C1) ecotypes, with differences in carbohydrate utilization, defense systems, and chemotaxis, among other characteristics. Nonetheless, we identified frequent intra- and interspecies exchange of mobile genetic elements (e.g., antibiotic resistance plasmids, novel “chromids,” or two different and concurrent type VI secretion systems) that provide high levels of genetic diversity in the population. Surprisingly, we identified strains from both clusters in the mucosa of aquaculture species, indicating that manmade niches are bringing strains from the two clusters together. We propose an evolutionary model of V. vulnificus that could be broadly applicable to other pathogenic vibrios and facultative bacterial pathogens to pursue strategies to prevent their infections and emergence. IMPORTANCE Vibrio vulnificus is an emergent marine pathogen and is the cause of a deadly septicemia. However, the genetic factors that differentiate its clinical and environmental strains and its several biotypes remain mostly enigmatic. In this work, we investigated the underlying genomic properties and population dynamics of the V. vulnificus species to elucidate the traits that make these strains emerge as a human pathogen. The acquisition of different ecological determinants could have allowed the development of highly divergent clusters with different lifestyles within the same environment. However, we identified strains from both clusters in the mucosa of aquaculture species, indicating that manmade niches are bringing strains from the two clusters together, posing a potential risk of recombination and of emergence of novel variants. We propose a new evolutionary model that provides a perspective that could be broadly applicable to other pathogenic vibrios and facultative bacterial pathogens to pursue strategies to prevent their infections.
format	article
author	Mario López-Pérez Jane M. Jayakumar Jose M. Haro-Moreno Asier Zaragoza-Solas Geethika Reddi Francisco Rodriguez-Valera Orr H. Shapiro Munirul Alam Salvador Almagro-Moreno
author_facet	Mario López-Pérez Jane M. Jayakumar Jose M. Haro-Moreno Asier Zaragoza-Solas Geethika Reddi Francisco Rodriguez-Valera Orr H. Shapiro Munirul Alam Salvador Almagro-Moreno
author_sort	Mario López-Pérez
title	Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype
title_short	Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype
title_full	Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype
title_fullStr	Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype
title_full_unstemmed	Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype
title_sort	evolutionary model of cluster divergence of the emergent marine pathogen <italic toggle="yes">vibrio vulnificus</italic>: from genotype to ecotype
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/ba6067968c0c4b88b0a62c36491eb4bb
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Evolutionary Model of Cluster Divergence of the Emergent Marine Pathogen <italic toggle="yes">Vibrio vulnificus</italic>: From Genotype to Ecotype

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