Muller, Erinn M.

Ocean warming, disease, and pollution have contributed to global declines in coral abundances and diversity. In the Caribbean, corals previously dominated reefs, providing an architectural framework for diverse ecological habitats, but have significantly declined due to infectious disease and anthropogenic climate change. Key species like the coral Acropora cervicornis are critically endangered, prompting researchers to focus on scientific endeavors to identify factors influencing coral disease resistance and resilience. We previously showed that disease susceptibility, growth rates, and bleaching risk were all associated with the abundance of a single bacterial parasite, Candidatus Aquirickettsia rohweri which proliferates in vivo under nutrient enrichment. Yet how nutrients influence parasite physiology in vivo remains unknown. Here, we analyzed parasite gene expression from a disease-susceptible A. cervicornis genotype exposed to ambient or nutrient enrichment conditions. Electron microscopy showed that Ca. A. rohweri was abundant in coral tissue and densely packed in mucocytes prior to nutrient enrichment. Under ambient conditions, the parasite upregulated genes involved in translation, protein maintenance, and cell envelope integrity, consistent with a conserve-and-maintain strategy. Nutrient enrichment induced expression of genes associated with central metabolism, nutrient import, stress response, host interaction, and two-component systems. Together, these results indicate that nutrient enrichment activates a growth-and-exploitation strategy, likely exacerbating parasitic pressure on A. cervicornis .

Summary Holobiont phenotype results from a combination of host and symbiont genotypes as well as from prevailing environmental conditions that alter the relationships among symbiotic members. Corals exemplify this concept, where shifts in the algal symbiont community can lead to some corals becoming more or less thermally tolerant. Despite linkage between coral bleaching and disease, the roles of symbiotic bacteria in holobiont resistance and susceptibility to disease remains less well understood. This study thus characterizes the microbiome of disease‐resistant and ‐susceptible Acropora cervicornis coral genotypes (hereafter referred to simply as ‘genotypes’) before and after high temperature‐mediated bleaching. We found that the intracellular bacterial parasite ‘ Ca. Aquarickettsia rohweri’ was strikingly abundant in disease‐susceptible genotypes. Disease‐resistant genotypes, however, had notably more diverse and even communities, with correspondingly low abundances of ‘ Ca. Aquarickettsia’ . Bleaching caused a dramatic reduction of ‘ Ca. Aquarickettsia’ within disease‐susceptible corals and led to an increase in bacterial community dispersion, as well as the proliferation of opportunists. Our data support the hypothesis that ‘ Ca. Aquarickettsia’ species increase coral disease risk through two mechanisms: (i) the creation of host nutritional deficiencies leading to a compromised host‐symbiont state and (ii) the opening of niche space for potential pathogens during thermal stress.