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ABSTRACT Coral reefs have undergone extensive coral loss and shifts in community composition worldwide. Despite this, some coral species appear naturally more resistant, such asMadracis mirabilis(hereinMadracis).Madracishas emerged as the dominant hard coral in Curaçao, comprising 26% of coral cover in reefs that declined by 78% between 1973 and 2015. Although life history traits and competitive mechanisms contribute toMadracis’s success, these factors alone may not fully explain it, as other species with similar traits have not shown comparable success. Here, we investigated the potential role of microbial communities in the success ofMadracison Curaçao reefs by leveraging a low-bias bacterial and viral enrichment method for metagenomic sequencing of coral samples, resulting in 77 unique bacterial metagenome-assembled genomes and 2,820 viral genomic sequences. Our analyses showed thatMadracis-associated bacterial and viral communities are 12% and 20% richer than the communities of five sympatric coral species combined. TheMadracis-associated bacterial community was dominated byRuegeriaandSphingomonas, genera that have previously been associated with coral health, defense against pathogens, and bioremediation. These communities also displayed higher functional redundancy, which is often associated with ecological resilience. The viral community exhibited a 50% enrichment of proviruses relative to other corals. These proviruses had the genomic capacity to laterally transfer genes involved in antibiotic resistance, central metabolism, and oxidative stress responses, potentially enhancing the adaptive capacity of theMadracismicrobiome and contributing toMadracis’s success on Curaçao’s reefs. IMPORTANCEUnderstanding why some coral species persist and thrive while most are in fast decline is critical.Madracis mirabilisis increasingly dominant on degraded reefs in Curaçao, yet the role of microbial communities in its success remains underexplored. This study highlights the potential role ofMadracis-associated bacterial and viral communities in supporting coral resilience and competitive success. By identifying key microbial partners and viral genes that may enhance host stress tolerance and defense against pathogens, we broaden the understanding of how the coral holobiont contributes to species persistence under environmental stress. These insights are valuable for predicting key microbial community players in reef interactions and may inform microbiome-based strategies to support coral conservation and restoration. 

Abstract Background Predation pressure and herbivory exert cascading effects on coral reef health and stability. However, the extent of these cascading effects can vary considerably across space and time. This variability is likely a result of the complex interactions between coral reefs’ biotic and abiotic dimensions. A major biological component that has been poorly integrated into the reefs' trophic studies is the microbial community, despite its role in coral death and bleaching susceptibility. Viruses that infect bacteria can control microbial densities and may positively affect coral health by controlling microbialization. We hypothesize that viral predation of bacteria has analogous effects to the top-down pressure of macroorganisms on the trophic structure and reef health. Results Here, we investigated the relationships between live coral cover and viruses, bacteria, benthic algae, fish biomass, and water chemistry in 110 reefs spanning inhabited and uninhabited islands and atolls across the Pacific Ocean. Statistical learning showed that the abundance of turf algae, viruses, and bacteria, in that order, were the variables best predicting the variance in coral cover. While fish biomass was not a strong predictor of coral cover, the relationship between fish and corals became apparent when analyzed in the context of viral predation: high coral cover (> 50%) occurred on reefs with a combination of high predator fish biomass (sum of sharks and piscivores > 200 g m −2 ) and high virus-to-bacteria ratios (> 10), an indicator of viral predation pressure. However, these relationships were non-linear, with reefs at the higher and lower ends of the coral cover continuum displaying a narrow combination of abiotic and biotic variables, while reefs at intermediate coral cover showed a wider range of parameter combinations. Conclusions The results presented here support the hypothesis that viral predation of bacteria is associated with high coral cover and, thus, coral health and stability. We propose that combined predation pressures from fishes and viruses control energy fluxes, inhibiting the detrimental accumulation of ecosystem energy in the microbial food web.