Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells

ABSTRACT Vibrio parahaemolyticus is a globally disseminated Gram-negative marine bacterium and the leading cause of seafood-borne acute gastroenteritis. Pathogenic bacterial isolates encode two type III secretion systems (T3SS), with the second system (T3SS2) considered the main virulence factor in...

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Autores principales: Marcela de Souza Santos, Kim Orth
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:067e75d8efd44009883bd76f1972d5122021-11-15T15:45:55ZIntracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells10.1128/mBio.01506-142150-7511https://doaj.org/article/067e75d8efd44009883bd76f1972d5122014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01506-14https://doaj.org/toc/2150-7511ABSTRACT Vibrio parahaemolyticus is a globally disseminated Gram-negative marine bacterium and the leading cause of seafood-borne acute gastroenteritis. Pathogenic bacterial isolates encode two type III secretion systems (T3SS), with the second system (T3SS2) considered the main virulence factor in mammalian hosts. For many decades, V. parahaemolyticus has been studied as an exclusively extracellular bacterium. However, the recent characterization of the T3SS2 effector protein VopC has suggested that this pathogen has the ability to invade, survive, and replicate within epithelial cells. Herein, we characterize this intracellular lifestyle in detail. We show that following internalization, V. parahaemolyticus is contained in vacuoles that develop into early endosomes, which subsequently mature into late endosomes. V. parahaemolyticus then escapes into the cytoplasm prior to vacuolar fusion with lysosomes. Vacuolar acidification is an important trigger for this escape. The cytoplasm serves as the pathogen’s primary intracellular replicative niche; cytosolic replication is rapid and robust, with cells often containing over 150 bacteria by the time of cell lysis. These results show how V. parahaemolyticus successfully establishes an intracellular lifestyle that could contribute to its survival and dissemination during infection. IMPORTANCE The marine bacterium V. parahaemolyticus is the leading cause worldwide of seafood-borne acute gastroenteritis. For decades, the pathogen has been studied exclusively as an extracellular bacterium. However, recent results have revealed the pathogen’s ability to invade and replicate within host cells. The present study is the first characterization of the V. parahaemolyticus’ intracellular lifestyle. Upon internalization, V. parahaemolyticus is contained in a vacuole that would in the normal course of events ultimately fuse with a lysosome, degrading the vacuole’s contents. The bacterium subverts this pathway, escaping into the cytoplasm prior to lysosomal fusion. Once in the cytoplasm, it replicates prolifically. Our study provides new insights into the strategies used by this globally disseminated pathogen to survive and proliferate within its host.Marcela de Souza SantosKim OrthAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Marcela de Souza Santos
Kim Orth
Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells
description ABSTRACT Vibrio parahaemolyticus is a globally disseminated Gram-negative marine bacterium and the leading cause of seafood-borne acute gastroenteritis. Pathogenic bacterial isolates encode two type III secretion systems (T3SS), with the second system (T3SS2) considered the main virulence factor in mammalian hosts. For many decades, V. parahaemolyticus has been studied as an exclusively extracellular bacterium. However, the recent characterization of the T3SS2 effector protein VopC has suggested that this pathogen has the ability to invade, survive, and replicate within epithelial cells. Herein, we characterize this intracellular lifestyle in detail. We show that following internalization, V. parahaemolyticus is contained in vacuoles that develop into early endosomes, which subsequently mature into late endosomes. V. parahaemolyticus then escapes into the cytoplasm prior to vacuolar fusion with lysosomes. Vacuolar acidification is an important trigger for this escape. The cytoplasm serves as the pathogen’s primary intracellular replicative niche; cytosolic replication is rapid and robust, with cells often containing over 150 bacteria by the time of cell lysis. These results show how V. parahaemolyticus successfully establishes an intracellular lifestyle that could contribute to its survival and dissemination during infection. IMPORTANCE The marine bacterium V. parahaemolyticus is the leading cause worldwide of seafood-borne acute gastroenteritis. For decades, the pathogen has been studied exclusively as an extracellular bacterium. However, recent results have revealed the pathogen’s ability to invade and replicate within host cells. The present study is the first characterization of the V. parahaemolyticus’ intracellular lifestyle. Upon internalization, V. parahaemolyticus is contained in a vacuole that would in the normal course of events ultimately fuse with a lysosome, degrading the vacuole’s contents. The bacterium subverts this pathway, escaping into the cytoplasm prior to lysosomal fusion. Once in the cytoplasm, it replicates prolifically. Our study provides new insights into the strategies used by this globally disseminated pathogen to survive and proliferate within its host.
format article
author Marcela de Souza Santos
Kim Orth
author_facet Marcela de Souza Santos
Kim Orth
author_sort Marcela de Souza Santos
title Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells
title_short Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells
title_full Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells
title_fullStr Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells
title_full_unstemmed Intracellular <named-content content-type="genus-species">Vibrio parahaemolyticus</named-content> Escapes the Vacuole and Establishes a Replicative Niche in the Cytosol of Epithelial Cells
title_sort intracellular <named-content content-type="genus-species">vibrio parahaemolyticus</named-content> escapes the vacuole and establishes a replicative niche in the cytosol of epithelial cells
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/067e75d8efd44009883bd76f1972d512
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AT kimorth intracellularnamedcontentcontenttypegenusspeciesvibrioparahaemolyticusnamedcontentescapesthevacuoleandestablishesareplicativenicheinthecytosolofepithelialcells
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