Species-specific mechanisms of cytotoxicity toward immune cells determine the successful outcome of Vibrio infections

Type Article
Date 2019-07
Language English
Author(s) Rubio Tristan6, Oyanedel Daniel6, Labreuche Yannick2, 3, Toulza Eve7, Luo Xing4, Bruto Maxime3, Chaparro Cristian8, Torres MartaORCID1, 4, 5, de Lorgeril JulienORCID1, Haffner Philippe1, Vidal-Dupiol JeremieORCID1, Lagorce Arnaud6, Petton Bruno2, Mitta Guillaume7, Jacq Annick4, Le Roux Frederique2, 3, Charriere Guillaume6, Destoumieux-Garzon Delphine8
Affiliation(s) 1 : Univ Montpellier, IFREMER, IHPE, CNRS, Univ Perpignan Via Domitia, F-34090 Montpellier, France.
2 : IFREMER, Unite Physiol Fonct Organismes Marins, F-29280 Plouzane, France.
3 : Sorbonne Univ, Univ Pierre & Marie Curie Paris 06, Stn Biol Roscoff, UMR 8227,CNRS,Integrat Biol Marine Models, F-29688 Roscoff, France.
4 : Univ Paris Saclay, Univ Paris Sud, Inst Integrat Biol Cell Commissariat Energi Atom, CNRS, F-91198 Gif Sur Yvette, France.
5 : Univ Granada, Dept Microbiol, Fac Pharm, E-18071 Granada, Spain.
6 : Univ Montpellier, IFREMER, IHPE, CNRS, Univ Perpignan Via Domitia, F-34090 Montpellier, France.
7 : Univ Montpellier, IFREMER, IHPE, CNRS, Univ Perpignan Via Domitia, F-34090 Montpellier, France.
8 : Univ Montpellier, IFREMER, IHPE, CNRS, Univ Perpignan Via Domitia, F-34090 Montpellier, France.
Source Proceedings Of The National Academy Of Sciences Of The United States Of America (0027-8424) (Natl Acad Sciences), 2019-07 , Vol. 116 , N. 28 , P. 14238-14247
DOI 10.1073/pnas.1905747116
WOS© Times Cited 13
Keyword(s) T6SS, toxin, dual RNA-seq, cytolysis, pathogenesis
Abstract

Vibrio species cause infectious diseases in humans and animals, but they can also live as commensals within their host tissues. How Vibrio subverts the host defenses to mount a successful infection remains poorly understood, and this knowledge is critical for predicting and managing disease. Here, we have investigated the cellular and molecular mechanisms underpinning infection and colonization of 2 virulent Vibrio species in an ecologically relevant host model, oyster, to study interactions with marine Vibrio species. All Vibrio strains were recognized by the immune system, but only nonvirulent strains were controlled. We showed that virulent strains were cytotoxic to hemocytes, oyster immune cells. By analyzing host and bacterial transcriptional responses to infection, together with Vibrio gene knock-outs, we discovered that Vibrio crassostreae and Vibrio tasmaniensis use distinct mechanisms to cause hemocyte lysis. Whereas V. crassostreae cytotoxicity is dependent on a direct contact with hemocytes and requires an ancestral gene encoding a protein of unknown function, r5.7, V. tasmaniensis cytotoxicity is dependent on phagocytosis and requires intracellular secretion of T6SS effectors. We conclude that proliferation of commensal vibrios is controlled by the host immune system, preventing systemic infections in oysters, whereas the successful infection of virulent strains relies on Vibrio species-specific molecular determinants that converge to compromise host immune cell function, allowing evasion of the host immune system.

Full Text
File Pages Size Access
Publisher's official version 10 1 MB Open access
Appendix 36 2 MB Open access
Dataset S01 49 KB Open access
Dataset S02 266 KB Open access
Dataset S03 19 KB Open access
Dataset S04 25 KB Open access
Top of the page

How to cite 

Rubio Tristan, Oyanedel Daniel, Labreuche Yannick, Toulza Eve, Luo Xing, Bruto Maxime, Chaparro Cristian, Torres Marta, de Lorgeril Julien, Haffner Philippe, Vidal-Dupiol Jeremie, Lagorce Arnaud, Petton Bruno, Mitta Guillaume, Jacq Annick, Le Roux Frederique, Charriere Guillaume, Destoumieux-Garzon Delphine (2019). Species-specific mechanisms of cytotoxicity toward immune cells determine the successful outcome of Vibrio infections. Proceedings Of The National Academy Of Sciences Of The United States Of America, 116(28), 14238-14247. Publisher's official version : https://doi.org/10.1073/pnas.1905747116 , Open Access version : https://archimer.ifremer.fr/doc/00507/61837/