Vibrio Zinc-Metalloprotease Causes Photoinactivation of Coral Endosymbionts and Coral Tissue Lesions

Sussman, Meir; Mieog, Jos C.; Doyle, Jason; Victor, Steven; Willis, Bette L.; Bourne, David G.

doi:10.1371/journal.pone.0004511

Cited by 93 publications

(102 citation statements)

References 127 publications

(132 reference statements)

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“…In the Vc450 genome, there are 45 annotated proteases, 2 of which (VIC_003472 thermolysin/zinc-metalloprotease and VIC_002633 neutral protease precursor) have homologous regions with metalloproteases previously identified in V. coralliilyticus infection studies (Ben-Haim et al, 2003b;Sussman et al, 2009). Out of the 21 proteases identified in the Vc450 proteome, neither VIC_003472 nor VIC_002633 were detected.…”

Section: Resultsmentioning

confidence: 99%

“…V. coralliilyticus P1 (VcP1), isolated from diseased corals in the Great Barrier Reef, infects corals at 28-31 1C (Sussman et al, 2008). It has been speculated that a zinc-metalloprotease may be driving these infections (Ben-Haim et al, 2003a;Sussman et al, 2009); however, recent infection experiments using a zinc-metalloprotease mutant of VcP1 (vcpA) revealed no significant differences in pathogenicity (de Oliveira Santos et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

Kimes

Grim

Johnson³

et al. 2011

The ISME Journal

223

200

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Sea surface temperatures (SST) are rising because of global climate change. As a result, pathogenic Vibrio species that infect humans and marine organisms during warmer summer months are of growing concern. Coral reefs, in particular, are already experiencing unprecedented degradation worldwide due in part to infectious disease outbreaks and bleaching episodes that are exacerbated by increasing SST. For example, Vibrio coralliilyticus, a globally distributed bacterium associated with multiple coral diseases, infects corals at temperatures above 27 1C. The mechanisms underlying this temperature-dependent pathogenicity, however, are unknown. In this study, we identify potential virulence mechanisms using whole genome sequencing of V. coralliilyticus ATCC (American Type Culture Collection) BAA-450. Furthermore, we demonstrate direct temperature regulation of numerous virulence factors using proteomic analysis and bioassays. Virulence factors involved in motility, host degradation, secretion, antimicrobial resistance and transcriptional regulation are upregulated at the higher virulent temperature of 27 1C, concurrent with phenotypic changes in motility, antibiotic resistance, hemolysis, cytotoxicity and bioluminescence. These results provide evidence that temperature regulates multiple virulence mechanisms in V. coralliilyticus, independent of abundance. The ecological and biological significance of this temperature-dependent virulence response is reinforced by climate change models that predict tropical SST to consistently exceed 27 1C during the spring, summer and fall seasons. We propose V. coralliilyticus as a model Gram-negative bacterium to study temperature-dependent pathogenicity in Vibrio-related diseases.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

Kimes

Grim

Johnson³

et al. 2011

The ISME Journal

223

200

View full text Add to dashboard Cite

show abstract

“…To determine the chemical signal responsible for this response, we analyzed coral mucus using quantitative NMR (Tapiolas et al, 2013). The DMSP concentrations in mucus from healthy colonies collected on Davies Reef, were high, ranging from 11.9-14.8 ( ± 1.2) mM for P. damicornis and up to 62.2 (±2.0) mM for A. millepora, another coral species susceptible to V. coralliilyticus infection (Sussman et al, 2009). Additional chemotaxis experiments revealed that DMSP (15 mM), when used as the sole attractant, elicited a chemotactic response of comparable magnitude to P. damicornis mucus (I C,MAX B14; Figure 2a).…”

Section: Resultsmentioning

confidence: 99%

“…DMSP (DMSP Á HCl; C5H10SO2 Á HCl; TCI) was freshly prepared with FASW to make 15 mM, 45mM and 61 mM working solutions that closely corresponded to the amount of DMSP measured in the P. damicornis and A. millepora mucus samples. A. millepora was chosen as a second species to test because V. coralliilyticus is known to infect it as well (Sussman et al, 2009). These freshly prepared DMSP solutions as well as P. damicornis mucus collected from Davies Reef (Great Barrier Reef; preserved at À 80 1C (as described in the mucus collection section) and thawed on ice directly before experimental use; measured to contain 12-15 mM DMSP) and from corals maintained in the laboratory at MIT, A. millepora mucus from the Great Barrier Reef (containing 45-62 mM DMSP) and a FASW control were tested against overnight cultures of V. coralliilyticus.…”

Section: Diffusive Gradient Microfluidic Experimentsmentioning

confidence: 99%

A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals

et al. 2013

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Diseases are an emerging threat to ocean ecosystems. Coral reefs, in particular, are experiencing a worldwide decline because of disease and bleaching, which have been exacerbated by rising seawater temperatures. Yet, the ecological mechanisms behind most coral diseases remain unidentified. Here, we demonstrate that a coral pathogen, Vibrio coralliilyticus, uses chemotaxis and chemokinesis to target the mucus of its coral host, Pocillopora damicornis. A primary driver of this response is the host metabolite dimethylsulfoniopropionate (DMSP), a key element in the global sulfur cycle and a potent foraging cue throughout the marine food web. Coral mucus is rich in DMSP, and we found that DMSP alone elicits chemotactic responses of comparable intensity to whole mucus. Furthermore, in heat-stressed coral fragments, DMSP concentrations increased fivefold and the pathogen's chemotactic response was correspondingly enhanced. Intriguingly, despite being a rich source of carbon and sulfur, DMSP is not metabolized by the pathogen, suggesting that it is used purely as an infochemical for host location. These results reveal a new role for DMSP in coral disease, demonstrate the importance of chemical signaling and swimming behavior in the recruitment of pathogens to corals and highlight the impact of increased seawater temperatures on disease pathways.

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“…Analysis of the extracellular products from strain P1 revealed a predominant zinc-metalloprotease that was found to be a homolog of the Vibrio cholerae hemagglutinin-protease (Sussman et al, 2008). When purified from the other extracellular products, this zinc-metalloprotease was demonstrated to cause coral tissue damage within 18 h at 27 1C (Sussman et al, 2009). Metalloproteases have several catalytic activities related to virulence but little is known about the diversity of these potential virulence factors in coral pathogenic bacteria.…”

Section: Introductionmentioning

confidence: 99%

Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire

et al. 2011

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Vibrio coralliilyticus has been implicated as an important pathogen of coral species worldwide. In this study, the nearly complete genome of Vibrio coralliilyticus strain P1 (LMG23696) was sequenced and proteases implicated in virulence of the strain were specifically investigated. The genome sequence of P1 (5 513 256 bp in size) consisted of 5222 coding sequences and 58 RNA genes (53 tRNAs and at least 5 rRNAs). Seventeen metalloprotease and effector (vgrG, hlyA and hcp) genes were identified in the genome and expressed proteases were also detected in the secretome of P1. As the VcpA zinc-metalloprotease has been considered an important virulence factor of V. coralliilyticus, a vcpA deletion mutant was constructed to evaluate the effect of this gene in animal pathogenesis. Both wild-type and mutant (DvcpA) strains exhibited similar virulence characteristics that resulted in high mortality in Artemia and Drosophila pathogenicity bioassays and strong photosystem II inactivation of the coral dinoflagellate endosymbiont (Symbiodinium). In contrast, the DvcpA mutant demonstrated higher hemolytic activity and secreted 18 proteins not secreted by the wild type. These proteins included four types of metalloproteases, a chitinase, a hemolysin-related protein RbmC, the Hcp protein and 12 hypothetical proteins. Overall, the results of this study indicate that V. coralliilyticus strain P1 has a diverse virulence repertoire that possibly enables this bacterium to be an efficient animal pathogen.

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Vibrio Zinc-Metalloprotease Causes Photoinactivation of Coral Endosymbionts and Coral Tissue Lesions

Cited by 93 publications

References 127 publications

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus

A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals

Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire

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