Vibrio coralliilyticus

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Classification Higher Order Taxa: Bacteria; Proteobacteria; Gammaproteobacteria; Vibrionales; Vibrionaceae; Vibrio (1)

Species: V. coralliilyticus


Description and Significance Vibrio coralliilyticus is a Gram-negative, rod-shaped pathogen implicated in causing the temperature-regulated bleaching and tissue lysis in the common coral, Pocillopora damicornis, that are prevalent in both the Indian and Pacific Oceans (2). Vibrio coralliilyticus is also known to be the etiological agent for coral bleaching driven by Black Band Disease (BBD), a major burden on coral reef health in marine systems globally (9). As corals provide shelter for a wide variety of marine life, the disruption caused by Vibrio coralliilyticus to the symbiosis between corals and their photosynthetic endosymbionts, known as Zooxanthellae, is an important consideration to scientists during an era of rising ocean temperature (2).

The potential global impact of Vibrio coralliilyticus abundance on marine ecosystems guides scientific research focusing on uncovering the pathogenicity and virulence factors of the organism. The relevance of V. coralliilyticus pathology and its significant implications in global coral disease place greater focus of current research on efforts to characterize the genome of V. coralliilyticus (3), understand its behavior under growth conditions (6). Other attributes of V. coralliilyticus remain understudied specifically cell structure (4), metabolism (5) and ecosystem interaction (9).

The scientific community has since concluded that coral bleaching is linked to climate change (2). Recent studies have demonstrated that the virulent nature of V. coralliilyticus is a determinant factor in coral bleaching (2). Taken together, this knowledge provide a rationale for further study of V. coralliilyticus from a global change perspective. A better understanding of V. coralliilyticus structure, behavior, metabolism and pathogenicity could contribute to potential solutions for coral bleaching and the survival of marine habitats provided by corals such as P. damicornis.


Genome Structure The first complete genome of Vibrio coralliilyticus (strain OCN014) was sequenced from the isolated diseased Acropora cytherea coral near the western reef terrace of Palmyra Atoll (3). The genomic DNA was isolated using the phenol-chloroform extraction method (14) and sequenced through pyrosequencing at Honolulu, Hawaii, close to the original site of sample collection (3). The complete genome of Vibrio coralliilyticus consists of 5,732,794 base pairs with about 45.7% of G+C content (3).


Significant Cell Features The flagellum plays an essential role in the chemotactic virulence mechanisms of V. coralliilyticus by granting it a motile nature. The effect of motility on virulence was on examined by loss of function experiments that demonstrated a nonmotile mutant form of the bacteria lacking the flagellar expression gene fh1A was seen to be non-pathogenic (4). Specifically, the nonmotile mutant was unable to resume virulence adhesion and chemotaxis behaviors, which are necessary for coral infection of the common coral, P. damicornis (4).


Metabolism A recent study conducted nuclear magnetic resonance (NMR) on Vibrio coralliilyticus in order to examine the extracted endometabolome when placed in stressful conditions (5). When placed in high-density, low-nutrient conditions, lysed V. coralliilyticus cells were found to have produced metabolic compounds including maltose, ethanolamine and bioplastic-type compound (BTC), 2-butenoic acid, 2-carboxy-1-methylethyl ester (5). The authors of this study used this compound identification to characterize the acute nutrient limitations of V. coralliilyticus. The authors propose that the production of maltose and ethanolamine, both cell membrane components, indicate that V. coralliilyticus turns on its own cell wall or that of neighboring cells to acquire carbon or nitrogen (5). This study surveyed the endometabolome of V. coralliilyticus, proposing these specific metabolic markers for extreme stress faced by the organism (5). Such insights into V. coralliilyticus metabolic indicators establish an initial framework for understanding V. coralliilyticus under various environmental conditions.


Ecology Vibrio coralliilyticus is one of over 80 Vibrio species abundant in marine systems. Like other counterpart species of the Vibrio genus, Vibrio coralliilyticus prefers residence in warm waters (>18°C) with low salinity (<2.5% NaCl) (9). Due to its preferential optimal growth conditions Vibrio coralliilyticus demonstrates strong seasonality, with its abundance especially high during summer months (9). Vibrio coralliilyticus is present in coral reefs in major seawater bodies such as the Pacific, Atlantic, and Indian Ocean as well as the Caribbean, the Bahamas and the Red Sea, where BBD bacteria have been found.

Vibrio coralliilyticus has been identified as part of the consortium of microbes that are responsible for Black Band Disease (BBD), a plague affecting coral reefs globally (9). BBD can be characterized visibly by the invasive black mat that strips healthy coral tissue as it spreads over the colony leaving behind only a calcium carbonate skeleton, the remnant of a once diverse ecosystem (9). The diverse community of microbiota that comprise the black mat include other Vibrio subspecies populations, cyanobacteria as well as oxidizers and sulfur reducers (9).

Coral reefs contain a dynamic interaction of host and microbial systems. These relationships range from symbiotic to parasitic in the case of Vibrio coralliilyticus. Characterization of coral reef microbiology has demonstrated the impact of the environment on microbial interactions in the coral and in turn the microbes impact on coral health. Tout et al. shows that the coral population drastically changes due to changes in environmental conditions, this affects growth and promotes settings for the growth of once hard to grow microbe into a competitive grower (9). Additionally, multiple studies have concluded that the marine microbiome can be influenced by abiotic factors including the rising seawater temperature associated with global warming (9).

There is vested community interest in the impact of Vibrio coralliilyticus is present in coral reefs in major seawater bodies such as the Pacific, Atlantic, and Indian Ocean as well as the Caribbean, the Bahamas and the Red Sea, where BBD bacteria have been found on coral health due to accepted scientific knowledge of rising seawater temperature linked to increasing pathogen-related bleaching effects (2). The effect of environmental condition on Vibrio coralliilyticus growth was demonstrated by Tout et al. who performed heat stress experiments where temperature was incrementally increased by two to three degrees to simulate environmental changes. This led to a significant increase in in Vibrio coralliilyticus population by at four orders of magnitude found by performing 16S amplicon sequencing and quantitative PCR targeting (9).

The discovery of novel non-genomic plasmids in Vibrio coralliilyticus has suggested that horizontal gene transfer may also aid in the survival and propagation of Vibrio coralliilyticus in particular ecological niches (10). Two ecological islands were found in addition to two open reading frames (10). These may encode for proteins that cooperate with genomically encoded proteins help Vibrio coralliilyticus in more environments by increasing nutrient options (10).


Pathology The genomic sequencing of V. coralliilyticus BAA-450 strain revealed protein coding genes involved in virulence signaling (6). One of the characterized genes encodes for a bacterial thermosensor. Kimes et al. showed that an increase in temperature from 24 °C to 27 °C activates the V. coralliilyticus thermosensor which in turn causes expression of additional V. coralliilyticus virulence proteins (6). Ultimately the V. coralliilyticus thermosensor is able to initiate the expression of downstream virulence proteins.

As discussed above, non-motile V. coralliilyticus mutants were found to be wholly non-pathogenic, emphasizing the essential role of the flagella in mediating motility, chemotaxis and by extension, virulence, as (4). Additionally, an examination of V. coralliilyticus temperature-dependent gene expression demonstrated upregulation of virulence genes involved in antimicrobial resistance, secretion systems and flagellar-mediated motility (7).

A common group of virulence factors produced by V. coralliilyticus include zinc-metalloproteases, shown to cause photoinactivation of coral endosymbionts and coral tissue lesions (7). While the identity of these virulence factors have been known for several years, their characterization in V. coralliilyticus is more recent. With this aim qRT-PCR primers were designed to specifically measure vpcA zinc-metalloprotease transcript in coral samples (8). In the future, this method could be used to understand the molecular mechanism by which V. coralliilyticus vpcA zinc-metalloprotease functions in coral bleaching.

In an aim to understand the role of V. coralliilyticus in coral bleaching in a changing environment, Tout et al. measured the V. coralliilyticus 16S rRNA abundance in coral samples after heat-bleaching, revealing that increases in seawater temperatures and associated P. damicornis bleaching were correlated with a 2-3 fold increase in V. coralliilyticus abundance (9). The finding that temperature rises promote V. coralliilyticus growth in coral demonstrates the ecological significance of this species’ virulence within a warming world.


Current Research Understanding the mechanisms driving V. coralliilyticus pathology underpin current scientific research on the subject. Given the potential burden of V. coralliilyticus on global coral populations, especially within a changing climate, pathology and virulence are of particular concern.

In this process, however, it appears that literature investigating basic cell structure, behavior and function not directly linked to virulence have remained on the fringe. For example, Winn et al. examined the chemotactic search pattern preference of V. coralliilyticus under various levels of oxygen availability (14). This study found that V. coralliilyticus maintained motility in both oxic and anoxic conditions, but that the 3-step flick chemotactic search pattern occurred only in oxic conditions, indicating a behavioral change in response to its environment (14). The behavioral findings of Winn et al. could be significant in eventually understanding V. coralliilyticus virulence, though this type of study certainly does not dominate mainstream pathology research on V. coralliilyticus.

An area garnering attention in the scientific community is a focus on how to best model this marine system research in the laboratory. Coral belongs to a cnidarian phylum that is comprised of about 10,000 aquatic organisms including jellyfish, hydras and sea anemones (11). As a means to model the cnidarian pathogenicity, Gilmore et al. had shown that V. coralliilyticus directs Toll-like receptor (TLR) activation in Starlet sea anemone also known as Nematostella ventensis (12). TLRs are pathogen recognition receptors involved in expression of innate immunity genes, however TLRs function in simple marine invertebrates is not well understood. In that TLR recognition of V. coralliilyticus in N. ventensis provided a molecular insight in understanding pathogen response in cnidarian.

Some recent efforts have involved the investigation of potential therapies for V. coralliilyticus pathology. In fact, bacteriophage YC was found to have the potential to prevent the pathogenicity of V. coralliilyticus in corals (15). Bacteriophage YC is a lytic phage of the Myoviridae family first isolated from the same area as V. coralliilyticus was first isolated: Nelly Bay, Magnetic Island, central Great Barrier Reef (GBR). Phage therapy studies show that bacteriophage YC infects V. coralliilyticus and inhibits induced tissue lysis and photoinactivation (15). These results point to the use of bacteriophage YC as a potential treatment for coral bleaching and V. coralliilyticus pathology in the marine environment (15).


References

1) Ben-Haim Y and Rosenberg E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Marine Biology, 141(1), 47-55.

2) Rozenblat YB and Rosenberg E (2004). Temperature-regulated bleaching and tissue lysis of Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Coral Health and Disease, 301-324.

3) Ushijima B, Videau P, Poscablo D et al (2014). Complete genome sequence of Vibrio coralliilyticus strain OCN014, isolated from a diseased coral at Palmyra Atoll. Genome Announcements, 2(6), e01318-14.

4) Meron D, Efrony R, Johnson WR et al (2015). Role of flagella in virulence of the coral pathogen Vibrio coralliilyticus. Applied and Environmental Microbiology, 75(17), 5704-5707.

5) Boroujerdi AF, Jones SS, Bearden DW et al (2012). NMR analysis of metabolic responses to extreme conditions of the temperature-dependent coral pathogen Vibrio coralliilyticus. Lett Applied Microbiology, 54(3), 209-216.

6) Kimes NE, Grim CJ, Johnson JR et al (2012). Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. The ISME Journal, 6.4, 835.

7) Sussman M, Mieog JC, Doyle J et al (2009). Vibrio zinc-metalloprotease causes photoinactivation of coral endosymbionts and coral tissue lesions. PLoS ONE, 4(2).

8) Wilson B, Muirhead A, Bazanella M et al (2013). An improved detection and quantification method for the coral pathogen Vibrio coralliilyticus.” PLoS ONE, 8(12).

9) Tout J, Siboni N, Messer LF et al (2015). Increased seawater temperature increases the abundance and alters the structure of natural Vibrio populations associated with the coral Pocillopora damicornis. Frontiers in Microbiology, 18(6), 432.


10) Wachter J and Stuart AH (2016). In silico analysis of a novel plasmid from the coral pathogen Vibrio coralliilyticus reveals two potential “ecological islands”. Microorganisms 4(1).

11) Swalla, Billie (2007). Faculty of 1000 evaluation for Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. F1000 - Post-Publication peer review of the biomedical literature.

12) Brennan JJ, Messerschmidt JL, Williams LM et al (2017). Sea anemone model has a single Toll-like receptor that can function in pathogen detection, NF-κB signal transduction, and development. Proceedings of the National Academy of Sciences, 114, 114(47).

13) Ushijima B, Videau P, Aeby GS et al (2013). Draft genome sequence of Vibrio coralliilyticus strain OCN008, isolated from Kāne‘ohe Bay, Hawai‘i. Genome Announc. 1(5).

Winn KM, Bourne DG and Mitchell JG (2013) Vibrio coralliilyticus search patterns across an oxygen gradient. PLoS ONE. 8(7).

14) Cohen Y, Pollock JF, Rosenberg E et al (2013). Phage therapy treatment of the coral pathogen Vibrio coralliilyticus. Microbiologyopen. 2(1), 64-74.