From cholera to corals: Viruses as drivers of virulence in a major coral bacterial pathogen

Weynberg, Karen D.; Voolstra, Christian R.; Neave, Matthew J.; Buerger, Patrick; Oppen, Madeleine J. H. van

doi:10.1038/srep17889

Cited by 69 publications

(68 citation statements)

References 61 publications

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“…This bacterium is a Bacteroidetes-affiliated intracellular symbionts of amoebae and may be an endosymbiont of a protist host within coral tissues . In summer, the coral-associated microbial community also contained a higher abundance of bacteria belonging to the genus Thalassotalea (previously Thalassomonas), which have previously been found in increased numbers in diseased and stressed corals (Sunagawa et al, 2009;Weynberg et al, 2016). In fact, T. loyana has been identified as the causative agent of a white plaguelike disease (Thompson, 2006).…”

Section: Seasonality Has Higher Impact On Coral Holobiont Than Uv Radmentioning

confidence: 99%

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

et al. 2018

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Environmental conditions are known to influence corals and their associated communities of microorganisms. However, our insights into the impacts of seasonal changes in ultraviolet radiation (UVR) on both coral physiology and microbiome remain very limited. To address this challenge, we maintained the coral Acropora muricata shaded from UVR or under ambient UVR levels during two contrasting seasons, i.e. summer and winter, and assessed the impact of UVR on the coral holobiont at each season. To this end, we analyzed the physiology (e.g., calcification, protein content, photosynthesis-related parameters) and coral microbiota composition, as well as the abundance and composition of the microbial communities and organic matter contents of the surrounding seawater. Our results show major seasonal effects on coral phenotype: (1) a lower host biomass and photosynthesizing, but fast calcifying phenotype in summer, and (2) a higher host biomass and photosynthesizing, but slow calcifying phenotype in winter. UVR had only a significant impact on Symbiodinium functioning. Specifically, high UVR levels reduced photosynthesis efficiency in summer, but an increase in chlorophyll a content may have compensated for this effect. The coral microbiota, which was variable but generally dominated by Endozoicomonas, was not affected by UVR, but its composition differed between seasons. In contrast, UVR had a major, but differential impact on the seawater microbial communities at both seasons. Particularly in summer, bacteria from the Alteromonadaceae were significantly more abundant (15-fold; up to 75%) in seawater under ambient UVR levels. Overall, our study suggests that UVR has only a limited impact on coral holobiont composition and functioning, despite major fluctuations in the surrounding seawater microbiome; seasonal changes in the holobiont are thus mostly driven by other environmental factors.

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Section: Seasonality Has Higher Impact On Coral Holobiont Than Uv Radmentioning

confidence: 99%

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

et al. 2018

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“…Phages are also capable of lysogenic conversion, which may contribute to pathogenesis of the disease through the introduction of new genetic information such as virulence genes into the genome of the pathogen (Brüssow, Canchaya, and Hardt 2004). This virally‐mediated pathogencity inducing mechanism has been suggested for the coral pathogen Vibrio coralliilyticus that causes some types of white syndromes (Weynberg et al ., ). Relevance of phages in BBD pathogenesis is further suggested by the genomes of BBD‐associated cyanobacteria harbouring CRISPR‐Cas systems, which defend against bacteriophage infections (Buerger et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Novel T4 bacteriophages associated with black band disease in corals

Buerger

Weynberg

Wood‐Charlson

et al. 2018

Environmental Microbiology

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Summary Research into causative agents underlying coral disease have focused primarily on bacteria, whereas potential roles of viruses have been largely unaddressed. Bacteriophages may contribute to diseases through the lysogenic introduction of virulence genes into bacteria, or prevent diseases through lysis of bacterial pathogens. To identify candidate phages that may influence the pathogenicity of black band disease (BBD), communities of bacteria (16S rRNA) and T4‐bacteriophages (gp23) were simultaneously profiled with amplicon sequencing among BBD‐lesions and healthy‐coral‐tissue of Montipora hispida, as well as seawater (study site: the central Great Barrier Reef). Bacterial community compositions were distinct among BBD‐lesions, healthy coral tissue and seawater samples, as observed in previous studies. Surprisingly, however, viral beta diversities based on both operational taxonomic unit (OTU)‐compositions and overall viral community compositions of assigned taxa did not differ statistically between the BBD‐lesions and healthy coral tissue. Nonetheless, relative abundances of three bacteriophage OTUs, affiliated to Cyanophage PRSM6 and Prochlorococcus phages P‐SSM2, were significantly higher in BBD‐lesions than in healthy tissue. These OTUs associated with BBD samples suggest the presence of bacteriophages that infect members of the cyanobacteria‐dominated BBD community, and thus have potential roles in BBD pathogenicity.

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“…However, important questions, such as the direct cause of BBD onset and progression drivers, remain unclear (Sato et al, 2016). Although the role of viruses, in particular bacteriophages, can provide new insights into the drivers and causation of a coral disease (Weynberg et al, 2015), BBD etiology has most commonly been studied by investigating the functions of associated bacteria, while the role of bacteriophages has not been considered.…”

Section: Introductionmentioning

confidence: 99%

“…The bacteriophage transfers genes that encode for one of the primary virulence factors, such as the cholera toxin (CT), and converts V. cholerae from a non-pathogenic to a pathogenic strain (Waldor and Mekalanos, 1996; Faruque and Mekalanos, 2003). Lysogenic conversion may also transform Vibrio coralliilyticus into a coral pathogen triggering the coral disease white syndrome, since some of its virulence factors are found on pathogenicity islands that contain toxin genes homologous to those of the V. cholerae prophage (Weynberg et al, 2015). …”

Section: Introductionmentioning

confidence: 99%

CRISPR-Cas Defense System and Potential Prophages in Cyanobacteria Associated with the Coral Black Band Disease

et al. 2016

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Understanding how pathogens maintain their virulence is critical to developing tools to mitigate disease in animal populations. We sequenced and assembled the first draft genome of Roseofilum reptotaenium AO1, the dominant cyanobacterium underlying pathogenicity of the virulent coral black band disease (BBD), and analyzed parts of the BBD-associated Geitlerinema sp. BBD_1991 genome in silico. Both cyanobacteria are equipped with an adaptive, heritable clustered regularly interspaced short palindromic repeats (CRISPR)-Cas defense system type I-D and have potential virulence genes located within several prophage regions. The defense system helps to prevent infection by viruses and mobile genetic elements via identification of short fingerprints of the intruding DNA, which are stored as templates in the bacterial genome, in so-called “CRISPRs.” Analysis of CRISPR target sequences (protospacers) revealed an unusually high number of self-targeting spacers in R. reptotaenium AO1 and extraordinary long CRIPSR arrays of up to 260 spacers in Geitlerinema sp. BBD_1991. The self-targeting spacers are unlikely to be a form of autoimmunity; instead these target an incomplete lysogenic bacteriophage. Lysogenic virus induction experiments with mitomycin C and UV light did not reveal an actively replicating virus population in R. reptotaenium AO1 cultures, suggesting that phage functionality is compromised or excision could be blocked by the CRISPR-Cas system. Potential prophages were identified in three regions of R. reptotaenium AO1 and five regions of Geitlerinema sp. BBD_1991, containing putative BBD relevant virulence genes, such as an NAD-dependent epimerase/dehydratase (a homolog in terms of functionality to the third and fourth most expressed gene in BBD), lysozyme/metalloendopeptidases and other lipopolysaccharide modification genes. To date, viruses have not been considered to be a component of the BBD consortium or a contributor to the virulence of R. reptotaenium AO1 and Geitlerinema sp. BBD_1991. We suggest that the presence of virulence genes in potential prophage regions, and the CRISPR-Cas defense systems are evidence of an arms race between the respective cyanobacteria and their bacteriophage predators. The presence of such a defense system likely reduces the number of successful bacteriophage infections and mortality in the cyanobacteria, facilitating the progress of BBD.

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From cholera to corals: Viruses as drivers of virulence in a major coral bacterial pathogen

Cited by 69 publications

References 61 publications

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

Ultra-Violet Radiation Has a Limited Impact on Seasonal Differences in the Acropora Muricata Holobiont

Novel T4 bacteriophages associated with black band disease in corals

CRISPR-Cas Defense System and Potential Prophages in Cyanobacteria Associated with the Coral Black Band Disease

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