Abstract
Previous studies of coral viruses have employed either microscopy or metagenomics, but few have attempted to comprehensively link the presence of a virus-like particle (VLP) to a genomic sequence. We conducted transmission electron microscopy imaging and virome analysis in tandem to characterize the most conspicuous viral types found within the dominant Pacific reef-building coral genus Acropora. Collections for this study inadvertently captured what we interpret as a natural outbreak of viral infection driven by aerial exposure of the reef flat coincident with heavy rainfall and concomitant mass bleaching. All experimental corals in this study had high titers of viral particles. Three of the dominant VLPs identified were observed in all tissue layers and budding out from the epidermis, including viruses that were ∼70, ∼120, and ∼150 nm in diameter; these VLPs all contained electron dense cores. These morphological traits are reminiscent of retroviruses, herpesviruses, and nucleocytoplasmic large DNA viruses (NCLDVs), respectively. Some 300–500 nm megavirus-like VLPs also were observed within and associated with dinoflagellate algal endosymbiont (Symbiodinium) cells. Abundant sequence similarities to a gammaretrovirus, herpesviruses, and members of the NCLDVs, based on a virome generated from five Acropora aspera colonies, corroborated these morphology-based identifications. Additionally sequence similarities to two diagnostic genes, a MutS and (based on re-annotation of sequences from another study) a DNA polymerase B gene, most closely resembled Pyramimonas orientalis virus, demonstrating the association of a cosmopolitan megavirus with Symbiodinium. We also identified several other virus-like particles in host tissues, along with sequences phylogenetically similar to circoviruses, phages, and filamentous viruses. This study suggests that viral outbreaks may be a common but previously undocumented component of natural bleaching events, particularly following repeated episodes of multiple environmental stressors.
Highlights
Viruses are abundant and diverse residents of stony coral colonies
Based on these congruent morphological and genomic data, we show that this outbreak consisted of four major viruses: an atypical herpes-like virus, a retrovirus similar to gamma-retroviruses, and two nucleocytoplasmic large DNA viruses (NCLDVs): one 150–180 nm virus-like particle (VLP) most similar to phycodnaviruses and associated with the host coral and another ∼300–500 nm NCLDV in the candidate Family Megaviridae and associated with resident Symbiodinium
Phylogenetic analysis of a DNA polymerase-like contig generated in this study indicates that it originates from an undescribed virus within the Herpesviridae that is most similar to mammalian gammaherpesviruses
Summary
Viruses (phages and eukaryotic viruses) are abundant and diverse residents of stony coral colonies (reviewed in Vega Thurber and Correa, 2011). These viruses likely play multiple, parasitic and commensal roles in the health of coral reefs (e.g., Wilson et al, 2005; van Oppen et al, 2009; Rosenberg and ZilberRosenberg, 2014; Bettarel et al, 2015; Weynberg et al, 2015). In other cases, transmission electron microscopy has revealed structures within corals that are highly indicative of massive viral infection (e.g., crystalline arrays, viral factories; Lawrence et al, 2014)
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