Potential role of viruses in white plague coral disease

Abstract

White plague (WP)-like diseases of tropical corals are implicated in reef decline worldwide, although their etiological cause is generally unknown. Studies thus far have focused on bacterial or eukaryotic pathogens as the source of these diseases; no studies have examined the role of viruses. Using a combination of transmission electron microscopy (TEM) and 454 pyrosequencing, we compared 24 viral metagenomes generated from Montastraea annularis corals showing signs of WP-like disease and/or bleaching, control conspecific corals, and adjacent seawater. TEM was used for visual inspection of diseased coral tissue. No bacteria were visually identified within diseased coral tissues, but viral particles and sequence similarities to eukaryotic circular Rep-encoding single-stranded DNA viruses and their associated satellites (SCSDVs) were abundant in WP diseased tissues. In contrast, sequence similarities to SCSDVs were not found in any healthy coral tissues, suggesting SCSDVs might have a role in WP disease. Furthermore, Herpesviridae gene signatures dominated healthy tissues, corroborating reports that herpes-like viruses infect all corals. Nucleocytoplasmic large DNA virus (NCLDV) sequences, similar to those recently identified in cultures of Symbiodinium (the algal symbionts of corals), were most common in bleached corals. This finding further implicates that these NCLDV viruses may have a role in bleaching, as suggested in previous studies. This study determined that a specific group of viruses is associated with diseased Caribbean corals and highlights the potential for viral disease in regional coral reef decline.

Figure 1

Locations of sampled tissue from M. annularis colonies of different health states. BD tissue was taken from ∼5 cm from the D tissue, where disease was progressing from the base of the coral colony. Seawater samples were taken ∼16 cm above BD and B coral colonies.

Figure 2

Mean percentage of similarities to viral families (and satellite DNAs) in metagenomes generated from different coral health states and seawater. Viral similarities that comprised ⩾4% of the total known eukaryotic viral similarities for a given sample type (a). The rare virome (b) or the viral similarities comprising <4% of the total known eukaryotic viral similarities detected for a given sample type.

Figure 3

Viral ‘groups' among different coral health states. The mean relative percentage of similarities to each viral type was lumped into ‘groups' based on their common evolutionary history. ‘NCLDVs' are nucleocytoplasmic large double-stranded DNA (dsDNA) viruses, which include Ascoviridae, Phycodnaviridae, Poxviridae and Mimiviridae. ‘SCSDVs' are small circular ssDNA viruses and their associated satellites and include: Nanoviridae, Circoviridae and Gemniviridae, and satellite DNAs. The ‘other' category includes similarities to all viral types not fitting into the two previous groups (that is, in this study: Herpesviridae, Papillomaviridae and Polydnaviridae).

Figure 4

Transmission electron micrograph of viral particles detected in diseased M. annularis tissues. A herpes-like viral particle approximately 180 nm in width (a). A pox-like viral particle, approximately 200 nm in length (b). A gemini-like particle approximately 40 nm length (c).