Changes in the diversity and functionality of viruses that can bleach healthy coral.

Coral microbiomes play a crucial role in maintaining the health and functionality of holobionts. Disruption in the equilibrium of holobionts, including bacteria, fungi, and archaea, can result in the bleaching of coral. However, little is known about the viruses that can infect holobionts in coral, especially bacteriophages. Here, we employed a combination of amplicon and metagenomic analyses on Acropora muricata and Galaxea astreata to investigate the diversity and functionality of viruses in healthy and bleached corals. Analysis showed that the alpha diversity of holobionts (bacteria, eukaryotes, zooxanthellae, and lysogenic and lytic viruses) was higher in bleached corals than that in healthy corals. Meanwhile, bleached corals exhibited a relatively higher abundance of specific viral classes, including Revtraviricetes, Arfiviricetes, Faserviricetes, Caudoviricetes, Herviviricetes, and Tectiliviricetes; moreover, we found that the expression levels of functional genes involved in carbon and sulfur metabolism were enriched. An increase in Vibrio abundance has been reported as a notable factor in coral bleaching; our analysis also revealed an increased abundance of Vibrio in bleached coral. Finally, bleached corals contained a higher abundance of Vibrio phages and encoded more virulence factor genes to increase the competitiveness of Vibrio after coral bleaching. In conclusion, we attempted to understand the causes of coral bleaching from the perspective of phage-bacteria-coral tripartite interaction.

Importance: Viruses, especially bacteriophages, outnumber other microorganisms by approximately 10-fold and represent the most abundant members of coral holobionts. Corals represent a model system for the study of symbiosis, the influence of viruses on organisms inhabiting healthy coral reef, the role of rapid horizontal gene transfer, and the expression of auxiliary metabolic genes. However, the least studied component of coral holobiont are viruses. Therefore, there is a critical need to investigate the viral community of viruses, and their functionality, in healthy and bleached coral. Here, we compared the composition and functionality of viruses in healthy and bleached corals and found that viruses may participate in the induction of coral bleaching by enhancing the expression of virulence genes and other auxiliary metabolic functions.