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Ecological diversification reveals routes of pathogen emergence in endemic Vibrio vulnificus populations
Pathogen emergence is a complex phenomenon that, despite its public health relevance, remains poorly understood. Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2021-10, Vol.118 (40), p.1-12 |
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description | Pathogen emergence is a complex phenomenon that, despite its public health relevance, remains poorly understood. Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains and the unique genetic traits that allow these clones to colonize the human host remain mostly unknown. We recently surveyed a large estuary in eastern Florida, where outbreaks of the disease frequently occur, and found endemic populations of the bacterium. We established two sampling sites and observed strong correlations between location and pathogenic potential. One site is significantly enriched with strains that belong to one phylogenomic cluster (C1) in which the majority of clinical strains belong. Interestingly, strains isolated from this site exhibit phenotypic traits associated with clinical outcomes, whereas strains from the second site belong to a cluster that rarely causes disease in humans (C2). Analyses of C1 genomes indicate unique genetic markers in the form of clinical-associated alleles with a potential role in virulence. Finally, metagenomic and physicochemical analyses of the sampling sites indicate that this marked cluster distribution and genetic traits are strongly associated with distinct biotic and abiotic factors (e.g., salinity, nutrients, or biodiversity), revealing how ecosystems generate selective pressures that facilitate the emergence of specific strains with pathogenic potential in a population. This knowledge can be applied to assess the risk of pathogen emergence from environmental sources and integrated toward the development of novel strategies for the prevention of future outbreaks. |
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Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains and the unique genetic traits that allow these clones to colonize the human host remain mostly unknown. We recently surveyed a large estuary in eastern Florida, where outbreaks of the disease frequently occur, and found endemic populations of the bacterium. We established two sampling sites and observed strong correlations between location and pathogenic potential. One site is significantly enriched with strains that belong to one phylogenomic cluster (C1) in which the majority of clinical strains belong. Interestingly, strains isolated from this site exhibit phenotypic traits associated with clinical outcomes, whereas strains from the second site belong to a cluster that rarely causes disease in humans (C2). Analyses of C1 genomes indicate unique genetic markers in the form of clinical-associated alleles with a potential role in virulence. Finally, metagenomic and physicochemical analyses of the sampling sites indicate that this marked cluster distribution and genetic traits are strongly associated with distinct biotic and abiotic factors (e.g., salinity, nutrients, or biodiversity), revealing how ecosystems generate selective pressures that facilitate the emergence of specific strains with pathogenic potential in a population. This knowledge can be applied to assess the risk of pathogen emergence from environmental sources and integrated toward the development of novel strategies for the prevention of future outbreaks.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2103470118</identifier><identifier>PMID: 34593634</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Abiotic factors ; Animals ; Bacteria ; Biodiversity ; Biological Sciences ; Clusters ; Ecosystem ; Endemic Diseases ; Estuaries ; Florida ; Genetic markers ; Genetic Markers - genetics ; Genomes ; Humans ; Metagenomics ; Nutrients ; Ostreidae - microbiology ; Outbreaks ; Pathogens ; Phenotype ; Phylogeny ; Physicochemical analysis ; Populations ; Public health ; Risk assessment ; Sampling ; Vibrio Infections - microbiology ; Vibrio vulnificus ; Vibrio vulnificus - genetics ; Vibrio vulnificus - pathogenicity ; Virulence ; Virulence - genetics</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2021-10, Vol.118 (40), p.1-12</ispartof><rights>Copyright National Academy of Sciences Oct 5, 2021</rights><rights>2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-22ccc936f22100adc7cf37cb0eb4f1b48140fb4a248d360ca46902e63bc1d2c73</citedby><cites>FETCH-LOGICAL-c443t-22ccc936f22100adc7cf37cb0eb4f1b48140fb4a248d360ca46902e63bc1d2c73</cites><orcidid>0000-0002-1121-1204 ; 0000-0002-3996-6780 ; 0000-0003-2013-3233 ; 0000-0003-0913-1093</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/27075974$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/27075974$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34593634$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>López-Pérez, Mario</creatorcontrib><creatorcontrib>Jayakumar, Jane M.</creatorcontrib><creatorcontrib>Grant, Trudy-Ann</creatorcontrib><creatorcontrib>Zaragoza-Solas, Asier</creatorcontrib><creatorcontrib>Cabello-Yeves, Pedro J.</creatorcontrib><creatorcontrib>Almagro-Moreno, Salvador</creatorcontrib><title>Ecological diversification reveals routes of pathogen emergence in endemic Vibrio vulnificus populations</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Pathogen emergence is a complex phenomenon that, despite its public health relevance, remains poorly understood. Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains and the unique genetic traits that allow these clones to colonize the human host remain mostly unknown. We recently surveyed a large estuary in eastern Florida, where outbreaks of the disease frequently occur, and found endemic populations of the bacterium. We established two sampling sites and observed strong correlations between location and pathogenic potential. One site is significantly enriched with strains that belong to one phylogenomic cluster (C1) in which the majority of clinical strains belong. Interestingly, strains isolated from this site exhibit phenotypic traits associated with clinical outcomes, whereas strains from the second site belong to a cluster that rarely causes disease in humans (C2). Analyses of C1 genomes indicate unique genetic markers in the form of clinical-associated alleles with a potential role in virulence. Finally, metagenomic and physicochemical analyses of the sampling sites indicate that this marked cluster distribution and genetic traits are strongly associated with distinct biotic and abiotic factors (e.g., salinity, nutrients, or biodiversity), revealing how ecosystems generate selective pressures that facilitate the emergence of specific strains with pathogenic potential in a population. 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Vibrio vulnificus, an emergent human pathogen, can cause a deadly septicaemia with over 50% mortality rate. To date, the ecological drivers that lead to the emergence of clinical strains and the unique genetic traits that allow these clones to colonize the human host remain mostly unknown. We recently surveyed a large estuary in eastern Florida, where outbreaks of the disease frequently occur, and found endemic populations of the bacterium. We established two sampling sites and observed strong correlations between location and pathogenic potential. One site is significantly enriched with strains that belong to one phylogenomic cluster (C1) in which the majority of clinical strains belong. Interestingly, strains isolated from this site exhibit phenotypic traits associated with clinical outcomes, whereas strains from the second site belong to a cluster that rarely causes disease in humans (C2). Analyses of C1 genomes indicate unique genetic markers in the form of clinical-associated alleles with a potential role in virulence. Finally, metagenomic and physicochemical analyses of the sampling sites indicate that this marked cluster distribution and genetic traits are strongly associated with distinct biotic and abiotic factors (e.g., salinity, nutrients, or biodiversity), revealing how ecosystems generate selective pressures that facilitate the emergence of specific strains with pathogenic potential in a population. 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subjects | Abiotic factors Animals Bacteria Biodiversity Biological Sciences Clusters Ecosystem Endemic Diseases Estuaries Florida Genetic markers Genetic Markers - genetics Genomes Humans Metagenomics Nutrients Ostreidae - microbiology Outbreaks Pathogens Phenotype Phylogeny Physicochemical analysis Populations Public health Risk assessment Sampling Vibrio Infections - microbiology Vibrio vulnificus Vibrio vulnificus - genetics Vibrio vulnificus - pathogenicity Virulence Virulence - genetics |
title | Ecological diversification reveals routes of pathogen emergence in endemic Vibrio vulnificus populations |
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