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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. 

Abstract Coral diseases contribute to the rapid decline in coral reefs worldwide, and yet coral bacterial pathogens have proved difficult to identify because 16S rRNA gene surveys typically identify tens to hundreds of disease‐associate bacteria as putative pathogens. An example is white band disease (WBD), which has killed up to 95% of the now‐endangered CaribbeanAcroporacorals since 1979, yet the pathogen is still unknown. The 16S rRNA gene surveys have identified hundreds of WBD‐associated bacterial amplicon sequencing variants (ASVs) from at least nine bacterial families with little consensus across studies. We conducted a multi‐year, multi‐site 16S rRNA gene sequencing comparison of 269 healthy and 143 WBD‐infectedAcropora cervicornisand used machine learning modelling to accurately predict disease outcomes and identify the top ASVs contributing to disease. Our ensemble ML models accurately predicted disease with greater than 97% accuracy and identified 19 disease‐associated ASVs and five healthy‐associated ASVs that were consistently differentially abundant across sampling periods. Using a tank‐based transmission experiment, we tested whether the 19 disease‐associated ASVs met the assumption of a pathogen and identified two pathogenic candidate ASVs—ASV25Cysteiniphilum litoraleand ASV8Vibriosp. to target for future isolation, cultivation, and confirmation of Henle‐Koch's postulate via transmission assays. 

Abstract Coral species in the genus Acropora are key ecological components of coral reefs worldwide and represent the most diverse genus of scleractinian corals. While key species of Indo-Pacific Acropora have annotated genomes, no annotated genome has been published for either of the two species of Caribbean Acropora. Here we present the first fully annotated genome of the endangered Caribbean staghorn coral, Acropora cervicornis. We assembled and annotated this genome using high-fidelity nanopore long-read sequencing with gene annotations validated with mRNA sequencing. The assembled genome size is 318 Mb, with 28,059 validated genes. Comparative genomic analyses with other Acropora revealed unique features in A. cervicornis, including contractions in immune pathways and expansions in signaling pathways. Phylogenetic analysis confirms previous findings showing that A. cervicornis diverged from Indo-Pacific relatives around 41 million years ago, with the closure of the western Tethys Sea, prior to the primary radiation of Indo-Pacific Acropora. This new A. cervicornis genome enriches our understanding of the speciose Acropora and addresses evolutionary inquiries concerning speciation and hybridization in this diverse clade. 

Abstract Although stability is relatively well understood in macro‐organisms, much less is known about its drivers in host–microbial systems where processes operating at multiple levels of biological organisation jointly regulate the microbiome.We conducted an experiment to examine the microbiome stability of three Caribbean corals (Acropora cervicornis,Pseudodiploria strigosaandPorites astreoides) by placing them in aquaria and exposing them to a pulse perturbation consisting of a large dose of broad‐spectrum antibiotics before transplanting them into the field.We found that coral hosts harboured persistent, species‐specific microbiomes. Stability was generally high but variable across coral species, withA. cervicornismicrobiomes displaying the lowest community turnover in both the non‐perturbed and the perturbed field transplants. Interestingly, the microbiome ofP. astreoideswas stable in the non‐perturbed field transplants, but unstable in the perturbed field transplants.A mathematical model of host–microbial dynamics helped resolve this paradox by showing that when microbiome regulation is driven by host sanctioning, both resistance and resilience to invasion are low and can lead to instability despite the high direct costs bourne by corals. Conversely, when microbiome regulation is mainly associated with microbial processes, both resistance and resilience to invasion are high and promote stability at no direct cost to corals. We suggest that corals that are mainly regulated by microbial processes can be likened to ‘glass cannons’ because the high stability they exhibit in the field is due to their microbiome's potent suppression of invasive microbes. However, these corals are susceptible to destabilisation when exposed to perturbations that target the vulnerable members of their microbiomes who are responsible for mounting such powerful attacks against invasive microbes. The differential patterns of stability exhibited byP. astreoidesacross perturbed and non‐perturbed field transplants suggest it is a ‘glass cannon’ whose microbiome is regulated by microbial processes, whereasA. cervicornis’ consistent patterns of stability suggest that its microbiome is mainly regulated by host‐level processes.Our results show that understanding how processes that operate at multiple levels of biological organisation interact to regulate microbiomes is critical for predicting the effects of environmental perturbations on host–microbial systems. 

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. 

Environmental compliance monitoring associated with the Port Miami dredging project (2013–2015), designed to assess the impact of project-generated sediments on the local coral community, fortuitously captured a thermal bleaching event and the first reports of an emergent, highly contagious, white-plague-like coral disease outbreak in the fall of 2014. The disease, now termed stony coral tissue loss disease (SCTLD), has decimated reefs throughout Florida and is now spreading across the Caribbean. The high prevalence of disease, the number of affected species, and the high mortality of corals affected suggests SCTLD may be the most lethal coral disease ever recorded. Previous analyses of the dredge monitoring data have reached mixed conclusions about the relative impact of dredging on coral mortality and has often parsed out disease susceptible individuals to isolate the impacts of dredging only. We use multi-variate analyses, including time-based survival analyses, to examine the timing and impacts of dredging, coral bleaching, and disease on local coral mortality. By examining the status of corals monthly from the October 2013 to July 2015 observational period, we found that coral mortality was not significantly affected by a coral’s proximity to the dredge site or sediment burial. Instead, coral mortality was most strongly impacted by disease and the emergence of SCTLD during the monitoring period. During the 2-year monitoring period, 26.3% of the monitored corals died, but the only conditions significantly affected by the dredge were partial burial and partial mortality. The strongest link to mortality was due to disease, which impacted coral species differently depending on their susceptibility to SCTLD. The focus on disturbances associated with dredging created a circumstance where the greater impacts of this emergent disease were downplayed, leading to a false narrative of the resulting mortality on the local coral communities. The results of this study reveal that while local events such as a dredging project do have quantifiable effects and can be harmful to corals, regional and global threats that result in mass coral mortality such as thermal stress and disease represent an existential threat to coral reefs and must be urgently addressed.