Viralization as a microbial approach for enhancing coral reef restoration.

Coral reef ecosystems rely on microorganisms to carry out biogeochemical processes essential to the survival of corals and the reef food web. However, widespread shifts from coral to algal dominance as a result of anthropogenic pressures have promoted microbial communities that compromise reef health through deoxygenation and disease. These degraded reefs become locked in a "microbialized" state characterized by high microbial biomass, low oxygen, and heightened pathogenic activity that stymie efforts to outplant corals onto the reef, a common approach applied to restore these ecosystems. Over 18 months, we compared viral and microbial dynamics alongside physical and chemical parameters ("water quality") between two coral outplanting sites and two midwater reef mesocosms called Coral Arks. Seafloor sites exhibited microbialization, whereas Arks maintained conditions with higher viral abundances and virus-to-microbe ratios, smaller and less abundant microorganisms, and consistently higher dissolved oxygen, water flow, and light availability. These conditions, which we term "viralized", supported enhanced coral growth and survival, greater benthic diversity, increased coral recruitment, reduced turf and macroalgae, and higher fish abundance compared to outplanting sites. Despite these benefits, analysis of microbial carbon metabolism genes revealed an underlying trend towards microbialization at both sites, reflecting larger-scale regional decline. These findings emphasize that microbial and physicochemical conditions are drivers of reef restoration outcomes; to be successful, restoration strategies must target the underlying environmental factors that support coral survival and resilience. We identify key microbial and physical variables-such as oxygen levels, flow, and viral activity-associated with viralized reef states, which should serve as focal points for developing new interventions and technologies aimed at creating conditions conducive to reef recovery.