Viral Outbreak in Corals Associated with an In Situ Bleaching Event: Atypical Herpes-Like Viruses and a New Megavirus Infecting Symbiodinium

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.

Rapid adaptive responses to climate change in corals

“…For example, shuffling of bacterial genes may result in wider metabolic potential, with coincident beneficial consequences for the coral host, for example, a broader range of products produced by dimethylsulfoniopropionate (DMSP)-metabolizing bacteria might enhance bacteria-mediated production of sulfur-based antimicrobials 97 . Despite such possible beneficial roles, however, viruses more typically have negative effects on host fitness and, in the case of corals, have been implicated in bleaching 98,99 and disease 100 .…”

Viruses in corals: hidden drivers of coral bleaching and disease?

“…Coral-associated virus communities are highly diverse and comprise bacteriophages, archaeal and eukaryotic viruses [10][11][12] . Despite this diversity, only a smaller subset of taxonomic groups are commonly found in corals, including bacteriophages belonging to the order of the Caudovirales, and eukaryotic nucleocytoplasmic large DNA viruses (NCLDVs) belonging to the families Phycodnaviridae, Mimiviridae, Poxviridae and Iridoviridae, as well as…”

A Student’s Guide to Giant Viruses Infecting Small Eukaryotes: From Acanthamoeba to Zooxanthellae

“…Indeed, their unique size and independence from host machinery may allow giant viruses to infect a wide range of hosts, which makes the search for the natural host more challenging. In addition to amoeba, NCLDVs have been reported to infect mice [46] and the symbiotic zooxanthelle of corals [47]. Giant viruses have also been isolated from human blood [48] and have been found in the human virome [49], indicating a potential role in human health (or at least a route of exposure).…”

“…Since the discovery of Mimivirus from a water cooling tower [86], giant viruses have been found in locations where amoebae normally thrive, including seawater, soil, aerosols, and man-made aquatic environments such as sewage, fountains and air conditioners [87], in addition to harsh, unexpected ecosystems such as permafrost [20]. Lastly, giant viruses or their DNA sequences have been observed in animals such as dinoflagellate-associated coral [47], arthropods, and humans [49,88]. …”

“…Major capsid gene phylogeny indicated the genes were likely from a Mimiviridae family member. Giant virus particles and marker genes have also recently also been observed associated with zooxanthellae from the genus Symbiodinium , a dinoflagellate typically found closely associated with corals [47]. Giant virus-like genes were also found in several other protists [133,135] and some plant genomes, namely Physcomitrella patens and Selaginella moellendorffii [136].…”