Reef invertebrate viromics: diversity, host specificity and functional capacity

Abstract

Recent metagenomic analyses have revealed a high diversity of viruses in the pelagic ocean and uncovered clear habitat-specific viral distribution patterns. Conversely, similar insights into the composition, host specificity and function of viruses associated with marine organisms have been limited by challenges associated with sampling and computational analysis. Here, we performed targeted viromic analysis of six coral reef invertebrate species and their surrounding seawater to deliver taxonomic and functional profiles of viruses associated with reef organisms. Sponges and corals' host species-specific viral assemblages with low sequence identity to known viral genomes. While core viral genes involved in capsid formation, tail structure and infection mechanisms were observed across all reef samples, auxiliary genes including those involved in herbicide resistance and viral pathogenesis pathways such as host immune suppression were differentially enriched in reef hosts. Utilising a novel OTU based assessment, we also show a prevalence of dsDNA viruses belonging to the Mimiviridae, Caudovirales and Phycodnaviridae in reef environments and further highlight the abundance of ssDNA viruses belonging to the Circoviridae, Parvoviridae, Bidnaviridae and Microviridae in reef invertebrates. These insights into coral reef viruses provide an important framework for future research into how viruses contribute to the health and evolution of reef organisms.

Thermal stress modifies the marine sponge virome

“…Under sub‐lethal acute heat stress, the virome of an abundant Great Barrier Reef sponge experiences a dramatic shift with a complete loss of ssDNA bacteriophage and an increase in endogenous retro‐transcribing viruses within the Caulimorviridae and Retroviridae families. Despite previous detection of AMGs that may provide competitive advantages to sponges (Weynberg et al ., ; Laffy et al ., ), we found no evidence for viral mediated introduction of metabolically advantageous genes to the sponge holobiont under thermal stress. The loss of particular ssDNA bacteriophage is likely due to loss of specific bacterial hosts, as R. odorabile has previously been reported to undergo dramatic microbial community shifts at 32 °C (Webster et al ., ; Fan et al ., ).…”

“…). No viral AMGs such as ‘cobalamin synthesis’ or ‘herbicide resistance,’ which were previously detected in sponge viromes (Laffy et al ., ) were evident in any sample from this study. Only four Swiss‐Prot keywords were exclusive to thermally stressed sponges: ‘long QT syndrome’, ‘antiviral defence’, ‘myosin’ and ‘lignin degradation’ (Fig.…”

“…Notable examples of viral symbioses include densovirus mediated introduction of pesticide resistance genes into the cotton bollworm genome (Xu et al ., ), gammaherpesvirus‐mediated resistance to bacterial infections in mice (Barton et al ., ) and integration of retroviral transposable elements into the promoters of stress response genes in yeast, increasing their expression under stress (Feng et al ., ). Functional metaviromic analysis has shown that some sponge‐associated viruses contain auxillary metabolic genes (AMGs) involved in processes such as cobalamin biosynthesis and herbicide resistance, which could also directly benefit the sponge host (Laffy et al ., ).…”

“…The partnership between sponges and their microbial and viral associates represents one of the most ancient examples of interkingdom symbiosis in multicellular life (Hentschel et al ., ). While the sponge microbiome has been intensively studied and reviewed numerous times (Taylor et al ., ; Taylor et al ., ; Webster and Blackall, ; Hentschel et al ., ; Webster and Taylor, ; Webster and Thomas, ; Pita et al ., ), the composition and function of the virome has only recently been elucidated (Laffy et al ., ; Laffy et al ., ; Pascelli et al ., ). Consistent with patterns in the microbiome, the sponge viral community is diverse and host‐species specific, being characterized by an abundance of the dsDNA order Caudovirales , ssDNA family Microviridae and representatives of the Megavirales including the Mimiviridae , Phycodnaviridae and Poxviridae families (Laffy et al ., ; Laffy et al ., ).…”

Indigenous versus Lessepsian Hosts: Nervous Necrosis Virus (NNV) in Eastern Mediterranean Sea Fish

“…Marine organisms typically host diverse communities of viruses, bacteria, archaea, and fungi [1][2][3]. Marine viruses are key drivers of host diversity, population dynamics, and biogeochemical cycles, and, therefore, their effect on the marine environment is extensive [2,4].…”