Coral-Associated Viral Assemblages From the Central Red Sea Align With Host Species and Contribute to Holobiont Genetic Diversity

Abstract

Coral reefs are highly diverse marine ecosystems increasingly threatened on a global scale. The foundation species of reef ecosystems are stony corals that depend on their symbiotic microalgae and bacteria for aspects of their metabolism, immunity, and environmental adaptation. Conversely, the function of viruses in coral biology is less well understood, and we are missing an understanding of the diversity and function of coral viruses, particularly in understudied regions such as the Red Sea. Here we characterized coral-associated viruses using a large metagenomic and metatranscriptomic survey across 101 cnidarian samples from the central Red Sea. While DNA and RNA viral composition was different across coral hosts, biological traits such as coral life history strategy correlated with patterns of viral diversity. Coral holobionts were broadly associated with Mimiviridae and Phycodnaviridae that presumably infect protists and algal cells, respectively. Further, Myoviridae and Siphoviridae presumably target members of the bacterial phyla Actinobacteria, Firmicutes, and Proteobacteria, whereas Hepadnaviridae and Retroviridae might infect the coral host. Genes involved in bacterial virulence and auxiliary metabolic genes were common among the viral sequences, corroborating a contribution of viruses to the holobiont's genetic diversity. Our work provides a first insight into Red Sea coral DNA and RNA viral assemblages and reveals that viral diversity is consistent with global coral virome patterns.

Keywords: Red Sea; coral; holobiont; metagenomics; metaorganism; metatranscriptomics; virus.

FIGURE 1

Coral viral community composition and diversity. Taxonomic profile of viral reads classified to the family level (left) and estimated number of viral families (right) found in coral (A) metagenomes and (B) metatranscriptomes. Barplots represent mean abundances of the 20 most abundant viral families annotated. Dendrograms represent hierarchical clustering on Bray-Curtis dissimilarities using Ward’s minimum variance method. Boxplots denote observed viral families.

FIGURE 2

Alignment of coral viral community composition and host traits. (A) Log10(1 + x)-transformed viral abundances of coral metagenomes and metatranscriptomes were constrained by host species using a distance-based redundancy analysis (RDA). Colors represent coral species and shapes represent host life history strategies. The percent variation explained by the RDA ordinations is indicated on the axes. (B) Heatmap of RDA inertia values for independent comparisons on each coral trait and the proportion of variance explained with regard to viral composition. Inertia values are Z-scaled and normalized within rows. MG stands for metagenomes and MT stands for metatranscriptomes.

FIGURE 3

Functional diversity of Red Sea coral-associated viruses. (A) Gene Ontology (GO) enriched biological processes in a two-level hierarchical structure. Contribution of higher order processes provided in percent at the top right; relative contribution of lower order provided in form of a pie chart. (B) Relative abundances of the 20 most abundant GO biological processes annotated to viral sequences across cnidarian metagenomes (top) and metatranscriptomes (bottom).