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ABSTRACT Coral reefs are increasingly threatened by disease outbreaks, yet little is known about the genetic mechanisms underlying disease resistance. Since the 1970s, White Band Disease (WBD) has decimated the Caribbean staghorn coralAcropora cervicornis. However, 15% or more of individuals are highly disease‐resistant, and the genes controlling the production of Argonaut proteins, involved in microRNA (miRNA) post‐transcriptional gene silencing, are up‐regulated in WBD‐resistant corals. This suggests that miRNAs may be key regulators of coral immunity. In this study, we conducted an in situ disease transmission experiment with five healthy‐exposed control tanks and five WBD‐exposed tanks, each containing 50A. cervicornisgenotypes, sampled over 7 days and then sequenced miRNAs from 12 replicate genotypes, including 12 WBD‐exposed and 12 healthy‐exposed control fragments from two time points. We identified 67bona fidemiRNAs inA. cervicornis, 3 of which are differentially expressed in disease‐resistant corals. We performed a phylogenetic comparison of miRNAs across cnidarians and found greater conservation of miRNAs in more closely related taxa, including all three differentially expressed miRNAs being conserved in more than oneAcroporacoral. One of the three miRNAs has putative genomic targets involved in the cnidarian innate immunity. In addition, community detection coupled with over‐representation analysis of our miRNA–messenger RNA (mRNA) target network found two key uniqueA. cervicornismiRNAs regulating multiple important immune‐related pathways such as Toll‐like receptor pathway, endocytosis, and apoptosis. These findings highlight how multiple miRNAs may help the coral host maintain immune homeostasis in the presence of environmental stress including disease. 

Diseases have caused unprecedent mortality in Caribbean coral communities. White band disease (WBD) has killed up to 95% of all endangered Caribbean Acroporids since it was first observed in 1979. Despite the devastating impacts of WBD, its etiology is currently unknown although recent research identified two bacterial strains – ASVs classified as aCysteiniphilum litoraleand aVibriosp., as the most likely pathogens. To better understand the disease etiology of WBD, we pretreated corals with antibiotics to determine how prophylactic use of antibiotics impacts the transmission of WBD in a replicated tank-based experiment. We found the prophylactic use of antibiotics led to significantly reduced infection rates in disease exposed corals with a 30-percentage point decrease in the infection rate. Analyses of 16S rRNA amplicon gene sequencing data in the disease exposed corals demonstrated that antibiotic pretreatment resulted in coral microbiomes which were less speciose and contained relatively fewerVibriospp. than untreated corals, indicating that the benefit of the antibiotic pretreatment was its ability to reduce the relative abundance of intrinsic secondary opportunists and/or opportunistic pathogens suggesting their likely importance to the etiology of WBD. We propose two distinct etiologies involving either an extrinsic keystone pathogen (Cysteiniphilum litorale) or overgrowth of intrinsic opportunistic pathogens (Vibriospp.). Future research should isolate these strains to confirm the etiology of white band disease. 

White band disease (WBD) has caused unprecedented declines in the CaribbeanAcroporacorals, which are now listed as critically endangered species. Highly disease-resistantAcropora cervicornisgenotypes exist, but the genetic underpinnings of disease resistance are not understood. Using transmission experiments, a newly assembled genome, and whole-genome resequencing of 76A. cervicornisgenotypes from Florida and Panama, we identified 10 genomic regions and 73 single-nucleotide polymorphisms that are associated with disease resistance and that include functional protein-coding changes in four genes involved in coral immunity and pathogen detection. Polygenic scores calculated from 10 genomic loci indicate that genetic screens can detect disease resistance in wild and nursery stocks ofA. cervicornisacross the Caribbean.