High microbial diversity, functional redundancy, and prophage enrichment support the success of the yellow pencil coral, Madracis mirabilis, in Curaçao's coral reefs.

Abstract

Coral reefs have undergone extensive coral loss and shifts in community composition worldwide. Despite this, some coral species appear naturally more resistant, such as Madracis mirabilis (herein Madracis). Madracis has 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 to Madracis'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 of Madracis on 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 that Madracis-associated bacterial and viral communities are 12% and 20% richer than the communities of five sympatric coral species combined. The Madracis-associated bacterial community was dominated by Ruegeria and Sphingomonas, 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 the Madracis microbiome and contributing to Madracis's success on Curaçao's reefs.

Importance: Understanding why some coral species persist and thrive while most are in fast decline is critical. Madracis mirabilis is increasingly dominant on degraded reefs in Curaçao, yet the role of microbial communities in its success remains underexplored. This study highlights the potential role of Madracis-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.