Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics

Recent studies revealed that several vibrio species have evolved the capacity to survive inside host cells. However, it is still often ignored if intracellular stages are required for pathogenicity. Virulence of Vibrio tasmaniensis LGP32, a strain pathogenic for Crassostrea gigas oysters, depends on...

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Published in:Environmental Microbiology
Main Authors: Vanhove, Audrey, Rubio, Tristan, Nguyen, An N., Lemire, Astrid, Roche, David, Nicod, Julie, Vergnes, Agnes, Poirier, Aurore, Disconzi, Elena, Bachere, Evelyne, Le Roux, Frederique, Jacq, Annick, Charriere, Guillaume, Destoumieux-garzon, Delphine
Format: Article in Journal/Newspaper
Language:English
Published: Wiley-blackwell 2016
Subjects:
Online Access:https://archimer.ifremer.fr/doc/00301/41254/88202.pdf
https://doi.org/10.1111/1462-2920.13083
https://archimer.ifremer.fr/doc/00301/41254/
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spelling ftarchimer:oai:archimer.ifremer.fr:41254 2023-05-15T15:58:40+02:00 Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics Vanhove, Audrey Rubio, Tristan Nguyen, An N. Lemire, Astrid Roche, David Nicod, Julie Vergnes, Agnes Poirier, Aurore Disconzi, Elena Bachere, Evelyne Le Roux, Frederique Jacq, Annick Charriere, Guillaume Destoumieux-garzon, Delphine 2016-03 application/pdf https://archimer.ifremer.fr/doc/00301/41254/88202.pdf https://doi.org/10.1111/1462-2920.13083 https://archimer.ifremer.fr/doc/00301/41254/ eng eng Wiley-blackwell https://archimer.ifremer.fr/doc/00301/41254/88202.pdf doi:10.1111/1462-2920.13083 https://archimer.ifremer.fr/doc/00301/41254/ 2015 Society for Applied Microbiology and John Wiley & Sons Ltd info:eu-repo/semantics/openAccess restricted use Environmental Microbiology (1462-2912) (Wiley-blackwell), 2016-03 , Vol. 18 , N. 3 , P. 875-888 text Publication info:eu-repo/semantics/article 2016 ftarchimer https://doi.org/10.1111/1462-2920.13083 2021-09-23T20:27:07Z Recent studies revealed that several vibrio species have evolved the capacity to survive inside host cells. However, it is still often ignored if intracellular stages are required for pathogenicity. Virulence of Vibrio tasmaniensis LGP32, a strain pathogenic for Crassostrea gigas oysters, depends on entry into hemocytes, the oyster immune cells. We investigated here the mechanisms of LGP32 intracellular survival and their consequences on the host–pathogen interaction. Entry and survival inside hemocytes were required for LGP32-driven cytolysis of hemocytes, both in vivo and in vitro. LGP32 intracellular stages showed a profound boost in metabolic activity and a major transcription of antioxidant and copper detoxification genes, as revealed by RNA sequencing. LGP32 isogenic mutants showed that resistance to oxidative stress and copper efflux are two main functions required for vibrio intracellular stages and cytotoxicity to hemocytes. Copper efflux was also essential for host colonization and virulence in vivo. Altogether, our results identify copper resistance as a major mechanism to resist killing by phagocytes, induce cytolysis of immune cells and colonize oysters. Selection of such resistance traits could arise from vibrio interactions with copper-rich environmental niches including marine invertebrates, which favour the emergence of pathogenic vibrios resistant to intraphagosomal killing across animal species. Article in Journal/Newspaper Crassostrea gigas Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Environmental Microbiology 18 3 875 888
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
description Recent studies revealed that several vibrio species have evolved the capacity to survive inside host cells. However, it is still often ignored if intracellular stages are required for pathogenicity. Virulence of Vibrio tasmaniensis LGP32, a strain pathogenic for Crassostrea gigas oysters, depends on entry into hemocytes, the oyster immune cells. We investigated here the mechanisms of LGP32 intracellular survival and their consequences on the host–pathogen interaction. Entry and survival inside hemocytes were required for LGP32-driven cytolysis of hemocytes, both in vivo and in vitro. LGP32 intracellular stages showed a profound boost in metabolic activity and a major transcription of antioxidant and copper detoxification genes, as revealed by RNA sequencing. LGP32 isogenic mutants showed that resistance to oxidative stress and copper efflux are two main functions required for vibrio intracellular stages and cytotoxicity to hemocytes. Copper efflux was also essential for host colonization and virulence in vivo. Altogether, our results identify copper resistance as a major mechanism to resist killing by phagocytes, induce cytolysis of immune cells and colonize oysters. Selection of such resistance traits could arise from vibrio interactions with copper-rich environmental niches including marine invertebrates, which favour the emergence of pathogenic vibrios resistant to intraphagosomal killing across animal species.
format Article in Journal/Newspaper
author Vanhove, Audrey
Rubio, Tristan
Nguyen, An N.
Lemire, Astrid
Roche, David
Nicod, Julie
Vergnes, Agnes
Poirier, Aurore
Disconzi, Elena
Bachere, Evelyne
Le Roux, Frederique
Jacq, Annick
Charriere, Guillaume
Destoumieux-garzon, Delphine
spellingShingle Vanhove, Audrey
Rubio, Tristan
Nguyen, An N.
Lemire, Astrid
Roche, David
Nicod, Julie
Vergnes, Agnes
Poirier, Aurore
Disconzi, Elena
Bachere, Evelyne
Le Roux, Frederique
Jacq, Annick
Charriere, Guillaume
Destoumieux-garzon, Delphine
Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
author_facet Vanhove, Audrey
Rubio, Tristan
Nguyen, An N.
Lemire, Astrid
Roche, David
Nicod, Julie
Vergnes, Agnes
Poirier, Aurore
Disconzi, Elena
Bachere, Evelyne
Le Roux, Frederique
Jacq, Annick
Charriere, Guillaume
Destoumieux-garzon, Delphine
author_sort Vanhove, Audrey
title Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
title_short Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
title_full Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
title_fullStr Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
title_full_unstemmed Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
title_sort copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics
publisher Wiley-blackwell
publishDate 2016
url https://archimer.ifremer.fr/doc/00301/41254/88202.pdf
https://doi.org/10.1111/1462-2920.13083
https://archimer.ifremer.fr/doc/00301/41254/
genre Crassostrea gigas
genre_facet Crassostrea gigas
op_source Environmental Microbiology (1462-2912) (Wiley-blackwell), 2016-03 , Vol. 18 , N. 3 , P. 875-888
op_relation https://archimer.ifremer.fr/doc/00301/41254/88202.pdf
doi:10.1111/1462-2920.13083
https://archimer.ifremer.fr/doc/00301/41254/
op_rights 2015 Society for Applied Microbiology and John Wiley & Sons Ltd
info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.1111/1462-2920.13083
container_title Environmental Microbiology
container_volume 18
container_issue 3
container_start_page 875
op_container_end_page 888
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