Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>

ABSTRACT Members of the genus Vibrio include many pathogens of humans and marine animals that share genetic information via horizontal gene transfer. Hence, the Vibrio pan-genome carries the potential to establish new pathogenic strains by sharing virulence determinants, many of which have yet to be...

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Autores principales:	Ann Ray, Lisa N. Kinch, Marcela de Souza Santos, Nick V. Grishin, Kim Orth, Dor Salomon
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ece9787ade514e03bc2fa8d7e3781f88
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spelling	oai:doaj.org-article:ece9787ade514e03bc2fa8d7e3781f882021-11-15T15:50:18ZProteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>10.1128/mBio.01077-162150-7511https://doaj.org/article/ece9787ade514e03bc2fa8d7e3781f882016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01077-16https://doaj.org/toc/2150-7511ABSTRACT Members of the genus Vibrio include many pathogens of humans and marine animals that share genetic information via horizontal gene transfer. Hence, the Vibrio pan-genome carries the potential to establish new pathogenic strains by sharing virulence determinants, many of which have yet to be characterized. Here, we investigated the virulence properties of Vibrio proteolyticus, a Gram-negative marine bacterium previously identified as part of the Vibrio consortium isolated from diseased corals. We found that V. proteolyticus causes actin cytoskeleton rearrangements followed by cell lysis in HeLa cells in a contact-independent manner. In search of the responsible virulence factor involved, we determined the V. proteolyticus secretome. This proteomics approach revealed various putative virulence factors, including active type VI secretion systems and effectors with virulence toxin domains; however, these type VI secretion systems were not responsible for the observed cytotoxic effects. Further examination of the V. proteolyticus secretome led us to hypothesize and subsequently demonstrate that a secreted hemolysin, belonging to a previously uncharacterized clan of the leukocidin superfamily, was the toxin responsible for the V. proteolyticus-mediated cytotoxicity in both HeLa cells and macrophages. Clearly, there remains an armory of yet-to-be-discovered virulence factors in the Vibrio pan-genome that will undoubtedly provide a wealth of knowledge on how a pathogen can manipulate host cells. IMPORTANCE The pan-genome of the genus Vibrio is a potential reservoir of unidentified toxins that can provide insight into how members of this genus have successfully risen as emerging pathogens worldwide. We focused on Vibrio proteolyticus, a marine bacterium that was previously implicated in virulence toward marine animals, and characterized its interaction with eukaryotic cells. We found that this bacterium causes actin cytoskeleton rearrangements and leads to cell death. Using a proteomics approach, we identified a previously unstudied member of the leukocidin family of pore-forming toxins as the virulence factor responsible for the observed cytotoxicity in eukaryotic cells, as well as a plethora of additional putative virulence factors secreted by this bacterium. Our findings reveal a functional new clan of the leukocidin toxin superfamily and establish this pathogen as a reservoir of potential toxins that can be used for biomedical applications.Ann RayLisa N. KinchMarcela de Souza SantosNick V. GrishinKim OrthDor SalomonAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Ann Ray Lisa N. Kinch Marcela de Souza Santos Nick V. Grishin Kim Orth Dor Salomon Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>
description	ABSTRACT Members of the genus Vibrio include many pathogens of humans and marine animals that share genetic information via horizontal gene transfer. Hence, the Vibrio pan-genome carries the potential to establish new pathogenic strains by sharing virulence determinants, many of which have yet to be characterized. Here, we investigated the virulence properties of Vibrio proteolyticus, a Gram-negative marine bacterium previously identified as part of the Vibrio consortium isolated from diseased corals. We found that V. proteolyticus causes actin cytoskeleton rearrangements followed by cell lysis in HeLa cells in a contact-independent manner. In search of the responsible virulence factor involved, we determined the V. proteolyticus secretome. This proteomics approach revealed various putative virulence factors, including active type VI secretion systems and effectors with virulence toxin domains; however, these type VI secretion systems were not responsible for the observed cytotoxic effects. Further examination of the V. proteolyticus secretome led us to hypothesize and subsequently demonstrate that a secreted hemolysin, belonging to a previously uncharacterized clan of the leukocidin superfamily, was the toxin responsible for the V. proteolyticus-mediated cytotoxicity in both HeLa cells and macrophages. Clearly, there remains an armory of yet-to-be-discovered virulence factors in the Vibrio pan-genome that will undoubtedly provide a wealth of knowledge on how a pathogen can manipulate host cells. IMPORTANCE The pan-genome of the genus Vibrio is a potential reservoir of unidentified toxins that can provide insight into how members of this genus have successfully risen as emerging pathogens worldwide. We focused on Vibrio proteolyticus, a marine bacterium that was previously implicated in virulence toward marine animals, and characterized its interaction with eukaryotic cells. We found that this bacterium causes actin cytoskeleton rearrangements and leads to cell death. Using a proteomics approach, we identified a previously unstudied member of the leukocidin family of pore-forming toxins as the virulence factor responsible for the observed cytotoxicity in eukaryotic cells, as well as a plethora of additional putative virulence factors secreted by this bacterium. Our findings reveal a functional new clan of the leukocidin toxin superfamily and establish this pathogen as a reservoir of potential toxins that can be used for biomedical applications.
format	article
author	Ann Ray Lisa N. Kinch Marcela de Souza Santos Nick V. Grishin Kim Orth Dor Salomon
author_facet	Ann Ray Lisa N. Kinch Marcela de Souza Santos Nick V. Grishin Kim Orth Dor Salomon
author_sort	Ann Ray
title	Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>
title_short	Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>
title_full	Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>
title_fullStr	Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>
title_full_unstemmed	Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>
title_sort	proteomics analysis reveals previously uncharacterized virulence factors in <named-content content-type="genus-species">vibrio proteolyticus</named-content>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/ece9787ade514e03bc2fa8d7e3781f88
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Proteomics Analysis Reveals Previously Uncharacterized Virulence Factors in <named-content content-type="genus-species">Vibrio proteolyticus</named-content>

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