Baums, Iliana B.

Abstract Microbes perform critical functions in corals, yet most knowledge is derived from the photic zone. Here, we discover two mollicutes that dominate the microbiome of the deep-sea octocoral, Callogorgia delta, and likely reside in the mesoglea. These symbionts are abundant across the host’s range, absent in the water, and appear to be rare in sediments. Unlike other mollicutes, they lack all known fermentative capabilities, including glycolysis, and can only generate energy from arginine provided by the coral host. Their genomes feature several mechanisms to interact with foreign DNA, including extensive CRISPR arrays and restriction-modification systems, which may indicate their role in symbiosis. We propose the novel family Oceanoplasmataceae which includes these symbionts and others associated with five marine invertebrate phyla. Its exceptionally broad host range suggests that the diversity of this enigmatic family remains largely undiscovered. Oceanoplasmataceae genomes are the most highly reduced among mollicutes, providing new insight into their reductive evolution and the roles of coral symbionts.

AbstractIn addition to abundant animal communities, corals from all ocean depths support diverse microbial associates that are important to coral health. While some of these microbes have been classified taxonomically, understanding the metabolic potential of coral-associated bacteria and how they interact with their coral hosts is limited by a lack of genomic data. One example is Mycoplasma and other members of the class Mollicutes which are widespread coral associates. Here we investigated the association between two novel members of the class Mollicutes and the deep-sea octocoral Callogorgia delta. We screened C. delta, a closely related species C. americana, sediment, and water for mollicutes using 16S metabarcoding. One ASV was found in most colonies screened (99/108) and often dominated the microbiome (up to 99%). Another ASV was detected at lower abundance and prevalence in these corals. Both were absent in all water and were absent or rare in the sediment. We sequenced metagenomes and metatranscriptomes to assemble and annotate genomes and propose the names Ca. Oceanoplasma callogorgiae and Ca. Thalassoplasma callogorgiae. The genomes were small, revealed a reliance on the arginine dihydrolase pathway for ATP production, and contained CRISPR-Cas systems with extensive arrays. CARD-FISH microscopy unveiled an abundant bacterium in the mesoglea which is likely to be Ca. O. callogorgiae. These novel mollicutes cluster with others from diverse invertebrate hosts. Altogether, this work describes the association of these novel mollicutes in C. delta, provides insight into widespread coral associates, and identifies a novel clade of marine mollicutes whose diversity remains largely undiscovered.

AbstractThe 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.

AbstractThe aquatic symbiont “Candidatus Aquarickettsia rohweri” infects a diversity of non-bilaterian metazoan phyla. In the threatened coral Acropora cervicornis, Aquarickettsia proliferates in response to increased nutrient exposure, resulting in suppressed growth and increased disease susceptibility and mortality. This study evaluated the extent, as well as the ecology and evolution of Aquarickettsia infecting the Caribbean corals: Ac. cervicornis and Ac. palmata and their hybrid (‘Ac. prolifera’). The bacterial parasite Aquarickettsia was found in all acroporids, with host and sampling location impacting infection magnitude. Phylogenomic and genome-wide single nucleotide variant analysis found Aquarickettsia clustering by region, not by coral taxon. Fixation analysis suggested within coral colonies, Aquarickettsia are genetically isolated to the extent that reinfection is unlikely. Relative to other Rickettsiales, Aquarickettsia is undergoing positive selection, with Florida populations experiencing greater positive selection relative to the other Caribbean locations. This may be due to Aquarickettsia response to increased nutrient stress in Florida, as indicated by greater in situ replication rates in these corals. Aquarickettsia did not significantly codiversify with either coral animal nor algal symbiont, and qPCR analysis of gametes and juveniles from susceptible coral genotypes indicated absence in early life stages. Thus, despite being an obligate parasite, Aquarickettsia must be horizontally transmitted via coral mucocytes, an unidentified secondary host, or a yet unexplored environmentally mediated mechanism. Importantly, the prevalence of Aquarickettsia in Ac. cervicornis and high abundance in Florida populations suggests that disease mitigation efforts in the US and Caribbean should focus on preventing early infection via horizontal transmission.