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

Type Article
Date 2016-03
Language English
Author(s) Vanhove Audrey1, Rubio Tristan1, Nguyen An N.2, Lemire Astrid3, 4, Roche David5, 6, Nicod Julie1, Vergnes Agnes1, Poirier Aurore1, Disconzi Elena2, Bachere Evelyne1, Le Roux Frederique3, 4, Jacq AnnickORCID, Charriere Guillaume1, Destoumieux-Garzon Delphine1
Affiliation(s) 1 : Univ Montpellier, Univ Perpignan, CNRS, IFREMER,IHPE,UMR 5244, Via Domitia, F-34095 Montpellier, France.
2 : Univ Paris 11, CNRS, CEA, I2BC, F-91405 Orsay, France.
3 : IFREMER, Unite Physiol Fonct Organismes Marins, CS 10070, F-29280 Plouzane, France.
4 : Univ Paris 06, Sorbonne Univ, Integrat Biol Marine Models, Stn Biol Roscoff,UMR 8227,CS 90074,CNRS, F-29688 Roscoff, France.
5 : Commissariat Energie Atom & Energies Alternat CEA, DSV, Inst Genom, Genoscope, F-91057 Evry, France.
6 : CNRS, Lab Anal Bioinformat Genom & Metab LABGeM, UMR 8030, F-91057 Evry, France.
Source Environmental Microbiology (1462-2912) (Wiley-blackwell), 2016-03 , Vol. 18 , N. 3 , P. 875-888
DOI 10.1111/1462-2920.13083
WOS© Times Cited 24
Note Special Issue: Special Issue on Pathogen Ecology
Abstract 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.
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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). Copper homeostasis at the host vibrio interface: lessons from intracellular vibrio transcriptomics. Environmental Microbiology, 18(3), 875-888. Publisher's official version : https://doi.org/10.1111/1462-2920.13083 , Open Access version : https://archimer.ifremer.fr/doc/00301/41254/