Outer membrane vesicles are vehicles for the delivery of<scp><i>V</i></scp><i>ibrio tasmaniensis</i>virulence factors to oyster immune cells

Vanhove, Audrey S.; Duperthuy, Marylise; Charrière, Guillaume M.; Roux, Frédérique Le; Goudenège, David; Gourbal, Benjamin; Kieffer‐Jaquinod, Sylvie; Couté, Yohann; Wai, Sun Nyunt; Destoumieux-Garzón, Delphine

doi:10.1111/1462-2920.12535

Cited by 71 publications

(88 citation statements)

References 69 publications

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“…Similarly, OmpU, the major OMP of Vibrio spp., plays roles in both pathogenesis and symbiosis within this genus (6,34). For instance, in pathogenic relationships, OmpU facilitates colonization (35), allowing binding to host tissue and inducing specific immune responses, including cell death (36)(37)(38). Conversely, in the mutualistic V. fischeri, although an ompU mutant has no growth defect in culture, it is only 60% as effective in the colonization process (39) and is compromised in the ability to avoid phagocytosis by the host's hemocytes (40), indicating a role for this OMP in the normal establishment and persistence of symbiosis.…”

Section: Discussionmentioning

confidence: 99%

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Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

et al. 2016

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Using the squid-vibrio association, we aimed to characterize the mechanism through which Vibrio fischeri cells signal morphogenesis of the symbiotic light-emitting organ. The symbiont releases two cell envelope molecules, peptidoglycan (PG) and lipopolysaccharide (LPS) that, within 12 h of light organ colonization, act in synergy to trigger normal tissue development. Recent work has shown that outer membrane vesicles (OMVs) produced by V. fischeri are sufficient to induce PG-dependent morphogenesis; however, the mechanism(s) of OMV release by these bacteria has not been described. Like several genera of both beneficial and pathogenic bacteria, V. fischeri cells elaborate polar flagella that are enclosed by an extension of the outer membrane, whose function remains unclear. Here, we present evidence that along with the well-recognized phenomenon of blebbing from the cell's surface, rotation of this sheathed flagellum also results in the release of OMVs. In addition, we demonstrate that most of the development-inducing LPS is associated with these OMVs and that the presence of the outer membrane protein OmpU but not the LPS O antigen on these OMVs is important in triggering normal host development. These results also present insights into a possible new mechanism of LPS release by pathogens with sheathed flagella. IMPORTANCEDetermining the function(s) of sheathed flagella in bacteria has been challenging, because no known mutation results only in the loss of this outer membrane-derived casing. Nevertheless, the presence of a sheathed flagellum in such host-associated genera as Vibrio, Helicobacter, and Brucella has led to several proposed functions, including physical protection of the flagella and masking of their immunogenic flagellins. Using the squid-vibrio light organ symbiosis, we demonstrate another role, that of V. fischeri cells require rotating flagella to induce apoptotic cell death within surface epithelium, which is a normal step in the organ's development. Further, we present evidence that this rotation releases apoptosis-triggering lipopolysaccharide in the form of outer membrane vesicles. Such release may also occur by pathogens but with different outcomes for the host.

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Section: Discussionmentioning

confidence: 99%

“…3) and that the rotating flagella of V. fischeri are a major source of these OMVs. It remains a mystery how the turning of the flagellum results in the release of OMVs; membrane blebs associated with the tip (13) or the shaft (35) (Fig. 6A) have been reported.…”

Section: Discussionmentioning

confidence: 99%

Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

et al. 2016

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“…The release of outer membrane vesicles (OMVs) is a sE-dependent mechanism [109], whose role in AMP resistance has been recently shown in vibrios. Vibrios, including the oyster pathogen V. tasmaniensis LGP32, were shown to release OMV protection against membrane-active AMPs [110,111]. Interestingly, OMV release was triggered by oyster plasma, suggesting, as shown in E. coli [112], that the membrane-active agents that are present in oyster plasma can trigger OMV release in vibrios.…”

Section: (Ii) Resistance To Amps In Vibriosmentioning

confidence: 99%

Antimicrobial peptides in marine invertebrate health and disease

Destoumieux-Garzón

Rosa

Schmitt

et al. 2016

Phil. Trans. R. Soc. B

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115

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One contribution of 13 to a theme issue 'Evolutionary ecology of arthropod antimicrobial peptides'. Aquaculture contributes more than one-third of the animal protein from marine sources worldwide. A significant proportion of aquaculture products are derived from marine protostomes that are commonly referred to as 'marine invertebrates'. Among them, penaeid shrimp (Ecdysozosoa, Arthropoda) and bivalve molluscs (Lophotrochozoa, Mollusca) are economically important. Mass rearing of arthropods and molluscs causes problems with pathogens in aquatic ecosystems that are exploited by humans. Remarkably, species of corals (Cnidaria) living in non-exploited ecosystems also suffer from devastating infectious diseases that display intriguing similarities with those affecting farmed animals. Infectious diseases affecting wild and farmed animals that are present in marine environments are predicted to increase in the future. This paper summarizes the role of the main pathogens and their interaction with host immunity, with a specific focus on antimicrobial peptides (AMPs) and pathogen resistance against AMPs. We provide a detailed review of penaeid shrimp AMPs and their role at the interface between the host and its resident/pathogenic microbiota. We also briefly describe the relevance of marine invertebrate AMPs in an applied context. This article is part of the themed issue 'Evolutionary ecology of arthropod antimicrobial peptides'.

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“…For example, infection with Vibrio tasmaniensis LGP32 [8] involves an intracellular phase in hemocytes, which are the oyster's immune-competent cells, and resistance to (i) antimicrobial peptides (AMPs), (ii) reactive oxygen species (ROS) and (iii) copper [9][10][11][12]. Vibrio aestuarianus, by [ 1 5 _ T D $ D I F F ] contrast, interacts with hemocytes extracellularly and inhibits their phagocytotic abilities [13,14].…”

Section: Involvement Of Vibrios In Oyster Diseasementioning

confidence: 99%

Oysters and Vibrios as a Model for Disease Dynamics in Wild Animals

Roux

Wegner

Polz

2016

Trends in Microbiology

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116

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Disease dynamics in the wild are influenced by a number of ecological and evolutionary factors not addressed by traditional laboratory-based characterization of pathogens. Here we propose the oyster, Crassostrea gigas, as a model for studying the interaction of the environment, bacterial pathogens, and the host in disease dynamics. We show that an important first step is to ask whether the functional unit of pathogenesis is a bacterial clone, a population, or a consortium in order to assess triggers of disease outbreaks and devise appropriate monitoring tools. Moreover, the development of specific-pathogen-free (SPF) oysters has enabled assessment of the infection process under natural conditions. Finally, recent results show the importance of microbial interactions and host genetics in determining oyster health and disease. Involvement of Vibrios in Oyster DiseaseVibrios are ubiquitous marine bacteria that are ecologically and metabolically diverse members of planktonic and animal-associated microbial communities [1,2]. They have been called 'opportuni-trophs ' [3] due to their high metabolic versatility and genetic variability coupled with chemotaxis and quorum sensing (see Glossary), all of which allow high colonization potential [4,5]. Vibrios encompass the ancient and well-studied human pathogen, Vibrio cholerae, as well as some less thoroughly characterized opportunistic pathogens capable of infecting humans, including Vibrio parahaemolyticus and Vibrio vulnificus [2]. Even less well understood are the consequences of Vibrio infections in other animals, including fish, coral, shrimp, and mollusks; however, infections in these organisms can have important environmental and economic consequences [6]. In particular, vibrios have been suggested to be responsible for repeated mortality outbreaks in oyster beds (Crassostrea gigas) in France that have resulted in losses of up to 80-100% of production (Box 1). However the onset and progression of disease in the wild has been difficult to follow in the past. Hence, it is often not clear whether vibrios isolated from diseased oysters are the causative agent, secondary opportunistic colonizers, or commensals [7].Vibrios appear to employ a diversity of molecular mechanisms to infect oysters, albeit our knowledge is based mainly on very few model strains. For example, infection with Vibrio tasmaniensis LGP32 [8] involves an intracellular phase in hemocytes, which are the oyster's immune-competent cells, and resistance to (i) antimicrobial peptides (AMPs), (ii) reactive oxygen species (ROS) and (iii) copper [9][10][11][12]. Vibrio aestuarianus, by [ 1 5 _ T D $ D I F F ] contrast, interacts with hemocytes extracellularly and inhibits their phagocytotic abilities [13,14]. A common theme, however, is that metalloproteases have been linked to toxicity in V. tasmaniensis, V. aestuarianus, Vibrio corallilyticus, and Vibrio tubiashi [13,15,16]. Nonetheless, the disruption of TrendsKnowledge of the genetic structure of the Vibrio population provides a framework for mapping d...

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Outer membrane vesicles are vehicles for the delivery ofVibrio tasmaniensisvirulence factors to oyster immune cells

Cited by 71 publications

References 69 publications

Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

Rotation of Vibrio fischeri Flagella Produces Outer Membrane Vesicles That Induce Host Development

Antimicrobial peptides in marine invertebrate health and disease

Oysters and Vibrios as a Model for Disease Dynamics in Wild Animals

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