Physiological responses of the scleractinian coral <i>Pocillopora damicornis</i> to bacterial stress from Vibrio coralliilyticus

Vidal-Dupiol, Jérémie; Ladrière, Ophélie; Meistertzheim, Anne-Leïla; Fouré, Laurent; Adjeroud, Mehdi; Mitta, Guillaume

doi:10.1242/jeb.053165

Cited by 89 publications

(102 citation statements)

References 100 publications

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“…These in situ measurements add a new dimension to existing evidence that some coral pathogens are chemotactic towards coral mucus and other host-derived compounds (Banin et al, 2001;Koren and Rosenberg, 2006;Rosenberg et al, 2007;Meron et al, 2009;Kimes et al, 2011;Vidal-Dupiol et al, 2011;Garren et al, 2014), and that chemotaxis and motility genes can be prominent and dynamic features in the metagenomes of coral-microbial communities (Vega Thurber et al, 2009). Given the strong chemotactic responses that we observed in the laboratory experiments and ISCA deployments, we propose that motility and chemotaxis may be important phenotypes within the context of coralmicrobial interactions.…”

Section: Discussionsupporting

confidence: 53%

Chemotaxis by natural populations of coral reef bacteria

et al. 2015

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Corals experience intimate associations with distinct populations of marine microorganisms, but the microbial behaviours underpinning these relationships are poorly understood. There is evidence that chemotaxis is pivotal to the infection process of corals by pathogenic bacteria, but this evidence is limited to experiments using cultured isolates under laboratory conditions. We measured the chemotactic capabilities of natural populations of coral-associated bacteria towards chemicals released by corals and their symbionts, including amino acids, carbohydrates, ammonium and dimethylsulfoniopropionate (DMSP). Laboratory experiments, using a modified capillary assay, and in situ measurements, using a novel microfabricated in situ chemotaxis assay, were employed to quantify the chemotactic responses of natural microbial assemblages on the Great Barrier Reef. Both approaches showed that bacteria associated with the surface of the coral species Pocillopora damicornis and Acropora aspera exhibited significant levels of chemotaxis, particularly towards DMSP and amino acids, and that these levels of chemotaxis were significantly higher than that of bacteria inhabiting nearby, non-coral-associated waters. This pattern was supported by a significantly higher abundance of chemotaxis and motility genes in metagenomes within coral-associated water types. The phylogenetic composition of the coral-associated chemotactic microorganisms, determined using 16S rRNA amplicon pyrosequencing, differed from the community in the seawater surrounding the coral and comprised known coral associates, including potentially pathogenic Vibrio species. These findings indicate that motility and chemotaxis are prevalent phenotypes among coral-associated bacteria, and we propose that chemotaxis has an important role in the establishment and maintenance of specific coral-microbe associations, which may ultimately influence the health and stability of the coral holobiont.

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Section: Discussionsupporting

confidence: 53%

Chemotaxis by natural populations of coral reef bacteria

et al. 2015

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“…This is in stark contrast to the association of temperature and disease state in strain BAA-450; at 27°C BAA-450 causes tissue loss in P. damicornis, whereas bleaching is observed at temperatures of 24 to 25°C (24). It has been suggested that BAA-450 invasion of P. damicornis cells occurs only at elevated water temperatures, perhaps accounting for tissue lysis only at temperatures above 27°C (49). Despite the differences in infection by the two strains, numerous genes encoding proteins that were upregulated in BAA-450 at elevated temperature (26) were also present in OCN008.…”

Section: Discussionmentioning

confidence: 86%

Vibrio coralliilyticus Strain OCN008 Is an Etiological Agent of Acute Montipora White Syndrome

Ushijima

Videau

Burger

et al. 2014

Appl Environ Microbiol

114

116

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dIdentification of a pathogen is a critical first step in the epidemiology and subsequent management of a disease. A limited number of pathogens have been identified for diseases contributing to the global decline of coral populations. Here we describe Vibrio coralliilyticus strain OCN008, which induces acute Montipora white syndrome (aMWS), a tissue loss disease responsible for substantial mortality of the coral Montipora capitata in Ka ne'ohe Bay, Hawai'i. OCN008 was grown in pure culture, recreated signs of disease in experimentally infected corals, and could be recovered after infection. In addition, strains similar to OCN008 were isolated from diseased coral from the field but not from healthy M. capitata. OCN008 repeatedly induced the loss of healthy M. capitata tissue from fragments under laboratory conditions with a minimum infectious dose of between 10 7 and 10 8 CFU/ml of water. In contrast, Porites compressa was not infected by OCN008, indicating the host specificity of the pathogen. A decrease in water temperature from 27 to 23°C affected the time to disease onset, but the risk of infection was not significantly reduced. Temperature-dependent bleaching, which has been observed with the V. coralliilyticus type strain BAA-450, was not observed during infection with OCN008. A comparison of the OCN008 genome to the genomes of pathogenic V. coralliilyticus strains BAA-450 and P1 revealed similar virulence-associated genes and quorum-sensing systems. Despite this genetic similarity, infections of M. capitata by OCN008 do not follow the paradigm for V. coralliilyticus infections established by the type strain.

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“…Bacterial stress was induced by the addition of V. coralliilyticus at 25°C, whereas bacterial infection was induced by the addition of V. coralliilyticus under conditions of increasing water temperature (from 25 to 32.5°C), which activated bacterial virulence. We recently reported that the bacterium becomes virulent at a temperature of 28°C (27).…”

Section: Stress Protocolmentioning

confidence: 99%

“…However, several recent studies have suggested the involvement of antibacterial agents. Thus, the mucus of several species of scleractinians has been shown to have antibacterial properties (23)(24)(25)(26), and in a recent study on the transcriptomic response of P. damicornis to its specific pathogenic bacterium V. coralliilyticus (27), we identified an mRNA corresponding to a putative antimicrobial peptide (AMP). 3 We describe here the isolation and characterization of damicornin, the first AMP reported from a scleractinian coral.…”

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confidence: 99%

Innate Immune Responses of a Scleractinian Coral to Vibriosis

Vidal-Dupiol

Ladrière

Destoumieux-Garzón

et al. 2011

Journal of Biological Chemistry

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102

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Scleractinian corals are the most basal eumetazoan taxon and provide the biological and physical framework for coral reefs, which are among the most diverse of all ecosystems. Over the past three decades and coincident with climate change, these phototrophic symbiotic organisms have been subject to increasingly frequent and severe diseases, which are now geographically widespread and a major threat to these ecosystems. Although coral immunity has been the subject of increasing study, the available information remains fragmentary, especially with respect to coral antimicrobial responses. In this study, we characterized damicornin from Pocillopora damicornis, the first scleractinian antimicrobial peptide (AMP) to be reported. We found that its precursor has a segmented organization comprising a signal peptide, an acidic proregion, and the C-terminal AMP. The 40-residue AMP is cationic, C-terminally amidated, and characterized by the presence of six cysteine molecules joined by three intramolecular disulfide bridges. Its cysteine array is common to another AMP and toxins from cnidarians; this suggests a common ancestor, as has been proposed for AMPs and toxins from arthropods. Damicornin was active in vitro against Gram-positive bacteria and the fungus Fusarium oxysporum. Damicornin expression was studied using a combination of immunohistochemistry, reverse phase HPLC, and quantitative RT-PCR. Our data show that damicornin is constitutively transcribed in ectodermal granular cells, where it is stored, and further released in response to nonpathogenic immune challenge. Damicornin gene expression was repressed by the coral pathogen Vibrio coralliilyticus. This is the first evidence of AMP gene repression in a host-Vibrio interaction.

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Physiological responses of the scleractinian coral Pocillopora damicornis to bacterial stress from Vibrio coralliilyticus

Cited by 89 publications

References 100 publications

Chemotaxis by natural populations of coral reef bacteria

Chemotaxis by natural populations of coral reef bacteria

Vibrio coralliilyticus Strain OCN008 Is an Etiological Agent of Acute Montipora White Syndrome

Innate Immune Responses of a Scleractinian Coral to Vibriosis

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