Muller, Erinn M

The critically endangered Caribbean staghorn coral Acropora cervicornis hosts microbiomes frequently dominated by the putatively parasitic intracellular bacterium Candidatus Aquirickettsia rohweri, which is associated with reduced coral growth and heightened disease susceptibility. Whether this dominance can be disrupted through antibiotic treatment and a sequential disturbance of thermal stress, remains unknown. In this study, we exposed disease-susceptible A. cervicornis fragments to broad-spectrum antibiotics, sub-bleaching thermal stress, or the combination of an antibiotic pre-treatment followed by thermal stress, and tracked changes in microbiome composition and diversity across all experimental phases using 16S rRNA amplicon sequencing and quantitative PCR (qPCR). We find that while the minor microbial fraction exhibits sustained compositional shifts in response to treatment, Ca. Aquirickettsia rohweri is resilient to antibiotic and thermal perturbation and may in fact increase in abundance following antibiotic exposure, suggesting that its dominance is actively maintained and not readily displaced by current disease mitigation strategies.These results indicate that antibiotic intervention is unlikely to be a viable strategy for disrupting Ca. A. rohweri dominance in disease-susceptible A. cervicornis, underscoring the urgency of understanding its transmission routes to inform microbiome rescue efforts.

Abstract The symbiont “Candidatus Aquarickettsia rohweri” infects a diversity of aquatic hosts. In the threatened Caribbean coral, Acropora cervicornis, Aquarickettsia proliferates in response to increased nutrient exposure, resulting in suppressed growth and increased disease susceptibility and mortality of coral. This study evaluated the extent, as well as the ecology and evolution of Aquarickettsia infecting threatened corals, Ac. cervicornis, and Ac. palmata and their hybrid (“Ac. prolifera”). Aquarickettsia was found in all acroporids, with coral host and geographic location impacting the infection magnitude. Phylogenomic and genome-wide single-nucleotide variant analysis of Aquarickettsia found phylogenetic clustering by geographic region, not by coral taxon. Analysis of Aquarickettsia fixation indices suggests multiple sequential infections of the same coral colony are unlikely. Furthermore, relative to other Rickettsiales species, Aquarickettsia is undergoing positive selection, with Florida populations experiencing greater positive selection relative to other Caribbean locations. This may be due in part to Aquarickettsia proliferating in response to greater nutrient stress in Florida, as indicated by greater in situ replication rates in these corals. Aquarickettsia was not found to significantly codiversify with either the coral animal or the coral’s algal symbiont (Symbiodinium “fitti”). Quantitative PCR analysis showed that gametes, larvae, recruits, and juveniles from susceptible, captive-reared coral genets were not infected with Aquarickettsia. Thus, horizontal transmission of Aquarickettsia via coral mucocytes or an unidentified host is more likely. The prevalence of Aquarickettsia in Ac. cervicornis and its high abundance in the Florida coral population suggests that coral disease mitigation efforts focus on preventing early infection via horizontal transmission.