The emergence of Vibrio pathogens in Europe: ecology, evolution, and pathogenesis (Paris, 11–12th March 2015)

Roux, Frédérique Le; Wegner, K. Mathias; Baker‐Austin, Craig; Vezzulli, Luigi; Osorio, Carlos R.; Amaro, Carmen; Ritchie, Jennifer M.; Defoirdt, Tom; Destoumieux-Garzón, Delphine; Blokesch, Melanie; Mazel, Didier; Jacq, Annick; Cava, Felipe; Gram, Lone; Wendling, Carolin Charlotte; Strauch, Eckhard; Kirschner, Alexander K. T.; Huehn, Stephan

doi:10.3389/fmicb.2015.00830

Cited by 120 publications

(97 citation statements)

References 90 publications

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“…The genetic diversity that we found among bacteria from the two sea bass farms in the Black Sea suggests that the infectious agent was already present in the environment, likely waiting for the appearance of stressful conditions, such as an increase in the water temperature, in order to cause infection. Global warming is causing bacterial species previously unreported in certain ecological areas to be increasingly reported and not only as mere environmental bacteria but as pathogens of either humans or animals or both (33). Actually, the pathogen was recovered from sea bass kidneys and spleens only in the period between July and October, i.e., in the warm season, with water temperatures ranging from 22.9 to 25.8°C at most sampling points.…”

Section: Discussionmentioning

confidence: 99%

Photobacterium damselae subsp. damselae, an Emerging Fish Pathogen in the Black Sea: Evidence of a Multiclonal Origin

Terceti

Öğüt

Osorio

2016

Appl Environ Microbiol

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Photobacterium damselae subsp. damselae is considered to be an emerging pathogen of marine fish of importance in aquaculture, with a notable increase in its geographical distribution during the last several years. In this study, we carried out for the first time to our knowledge a genetic and pathobiological characterization of 14 strains isolated from sea bass (Dicentrarchus labrax) reared in the Southeastern Black Sea, where high mortalities were observed at two aquaculture farms during the summer and autumn of 2011. Heterogeneity was evidenced among strains in phenotypical traits, such as sucrose fermentation, motility, and hemolysis. Although 11 of 14 isolates were hemolytic, we found that all of the isolates lacked the pPHDD1 virulence plasmid that encodes the phospholipase-D damselysin (Dly) and the pore-forming toxin PhlyP, two hemolysins previously reported to constitute major virulence factors for turbot. Subsequent PCR and sequencing analyses demonstrated that the 11 hemolytic isolates harbored a complete hlyA ch gene, a chromosome I-borne gene that encodes HlyA ch hemolysin, whereas the three nonhemolytic isolates contained hlyA ch pseudogenes caused by insertion sequence elements. Virulence challenges with two representative strains revealed that, albeit less virulent than the pPHDD1-harboring strain RM-71, the plasmidless hlyA ch -positive and hlyA chnegative Black Sea isolates were pathogenic for sea bass. A phylogenetic analysis based on the toxR gene sequence uncovered a greater diversity in the isolates, indicating that the presence of this pathogen in the Black Sea was not caused by the introduction and spread of a single virulent clone but by the proliferation of different clones. IMPORTANCEThe geographical distribution of marine bacterial pathogens is undergoing a worldwide increase. In particular, bacteria of the group vibrios are increasingly being isolated as the causative agents of disease in novel species of cultivated fish in areas where they had not been previously reported. Here we characterize for the first time to our knowledge a collection of isolates of the fish and human pathogen Photobacterium damselae subsp. damselae from diseased sea bass reared in the Black Sea. We uncovered great genetic diversity in the Black Sea isolates of this pathogen, suggesting a multiclonal origin. We also demonstrate for the first time that these isolates bear pathogenic potential for sea bass cultures by virulence challenges. P hotobacterium damselae subsp. damselae is a marine bacterium of the family Vibrionaceae that is recognized as a pathogen for a wide variety of aquatic animals, including fish, molluscs, and crustaceans. In addition, it is a pathogen of concern for humans, as it is capable of causing fatal infections (1). Most of the reported infections in humans originated from wounds inflicted during the handling of fish and fishing tools or from exposure to marine animals or seawater. Notably, it is a primary pathogen of fish species of economical importance in aquaculture. During ...

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Section: Discussionmentioning

confidence: 99%

Photobacterium damselae subsp. damselae, an Emerging Fish Pathogen in the Black Sea: Evidence of a Multiclonal Origin

Terceti

Öğüt

Osorio

2016

Appl Environ Microbiol

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“…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).…”

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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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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“…vulnificus case counts have increased over the past 15 years in the United States, and the infection is prevalent in endemic countries, including Japan, Taiwan, and South Korea [5, 11, 12]. Moreover, there is a growing risk of pathogen exposure in historically non-endemic areas as highlighted by case reports from countries including Sweden, Germany, France, and Denmark [13, 14]. Thus, the rise in V .…”

Section: Introductionmentioning

confidence: 99%

The Effector Domain Region of the Vibrio vulnificus MARTX Toxin Confers Biphasic Epithelial Barrier Disruption and Is Essential for Systemic Spread from the Intestine

2017

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Vibrio vulnificus causes highly lethal bacterial infections in which the Multifunctional Autoprocessing Repeats-in-Toxins (MARTX) toxin product of the rtxA1 gene is a key virulence factor. MARTX toxins are secreted proteins up to 5208 amino acids in size. Conserved MARTX N- and C-terminal repeat regions work in concert to form pores in eukaryotic cell membranes, through which the toxin’s central region of modular effector domains is translocated. Upon inositol hexakisphosphate-induced activation of the of the MARTX cysteine protease domain (CPD) in the eukaryotic cytosol, effector domains are released from the holotoxin by autoproteolytic activity. We previously reported that the native MARTX toxin effector domain repertoire is dispensable for epithelial cellular necrosis in vitro, but essential for cell rounding and apoptosis prior to necrotic cell death. Here we use an intragastric mouse model to demonstrate that the effector domain region is required for bacterial virulence during intragastric infection. The MARTX effector domain region is essential for bacterial dissemination from the intestine, but dissemination occurs in the absence of overt intestinal tissue pathology. We employ an in vitro model of V. vulnificus interaction with polarized colonic epithelial cells to show that the MARTX effector domain region induces rapid intestinal barrier dysfunction and increased paracellular permeability prior to onset of cell lysis. Together, these results negate the inherent assumption that observations of necrosis in vitro directly predict bacterial virulence, and indicate a paradigm shift in our conceptual understanding of MARTX toxin function during intestinal infection. Results implicate the MARTX effector domain region in mediating early bacterial dissemination from the intestine to distal organs–a key step in V. vulnificus foodborne pathogenesis–even before onset of overt intestinal pathology.

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The emergence of Vibrio pathogens in Europe: ecology, evolution, and pathogenesis (Paris, 11–12th March 2015)

Cited by 120 publications

References 90 publications

Photobacterium damselae subsp. damselae, an Emerging Fish Pathogen in the Black Sea: Evidence of a Multiclonal Origin

Photobacterium damselae subsp. damselae, an Emerging Fish Pathogen in the Black Sea: Evidence of a Multiclonal Origin

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

The Effector Domain Region of the Vibrio vulnificus MARTX Toxin Confers Biphasic Epithelial Barrier Disruption and Is Essential for Systemic Spread from the Intestine

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