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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 Corals (Cnidaria; Anthozoa) play critical roles as habitat-forming species with a wide range, from warm shallow-water tropical coral reefs to cold-water ecosystems. They also represent a complex ecosystem as intricate holobionts made up of microbes from all domains of the Tree of Life that can play significant roles in host health and fitness. The corallicolids are a clade of apicomplexans that infect a wide variety of anthozoans worldwide and can influence the thermal tolerance of habitat-forming corals. Despite their potentially important impacts on reef ecosystems, much of the basic biology and ecology of corallicolids remains unclear. Apicomplexans often have a closed life cycle, with minimal environmental exposure and sometimes multiple hosts. Corallicolids have only been documented in anthozoan hosts, with no known secondary/reservoir hosts or vectors. Here, we show that abundant corallicolid sequences are recovered from bearded fireworms (Hermodice carunculata) in tropical reef habitats off Curaçao and that they are distinct from corallicolids infecting the corals on which the fireworms were feeding at the time of their collection. These data are consistent with a fireworm-specific corallicolid infection, not merely a byproduct of the worms feeding on infected corals. Furthermore, we suggest that H. carunculata is potentially a vector moving corallicolids among coral hosts through its feces. These findings not only expand our understanding of the ecological interactions within coral reef ecosystems but also highlight the potential role of host-associated parasites in shaping the resilience of reef habitats.