Thurber, Rebecca Vega

Coral reefs are marine biodiversity hotspots that provide a wide range of ecosystem services. They are also reservoirs of bioactive compounds, many of which are produced by microbial symbionts associated with reef invertebrate hosts. However, for the keystone species of coral reefs, the reef-building corals themselves, we still lack a systematic assessment of their microbially encoded biosynthetic potential, and thus the molecular resources that may be at stake due to the alarming decline in reef biodiversity and cover. Here, we analysed microbial genomes reconstructed from 820 reef-building coral samples of three representative coral genera collected at 99 reefs across 32 islands during a two-year expedition throughout the Pacific Ocean (Tara Pacific). By contextualising our analyses with the microbiomes of other reef species, we found that genomic information was previously available for only 10% of the 4,224 microbial species overall and for less than 1% of the 645 species exclusively identified in Tara Pacific samples. We found reef-building coral microbiomes to be host-specific and their biosynthetic potential to rival or even surpass that found in traditional targets for natural product discovery, such as sponges and soft corals. Fire corals were not only particularly diverse in microbially encoded biosynthetic gene clusters (BGCs), but also in BGC-rich bacteria, including Acidobacteriota spp., which have been recently highlighted for their promising natural product repertoire. Together, this study unveils new candidate sources for bioactive compound discovery, prioritises targets for microbial isolation, and underscores the importance of conservation efforts by linking macro-organismal biodiversity loss to host-specific microbiomes and their biotechnological potential.

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.

AbstractThe aquatic symbiont “Candidatus Aquarickettsia rohweri” infects a diversity of non-bilaterian metazoan phyla. In the threatened coralAcropora cervicornis,Aquarickettsiaproliferates 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 ofAquarickettsiainfecting the Caribbean corals:Ac. cervicornisandAc. palmataand their hybrid (‘Ac. prolifera’). The bacterial parasiteAquarickettsiawas found in all acroporids, with host and sampling location impacting infection magnitude. Phylogenomic and genome-wide single nucleotide variant analysis foundAquarickettsiaclustering by region, not by coral taxon. Fixation analysis suggested within coral colonies,Aquarickettsiaare genetically isolated to the extent that reinfection is unlikely. Relative to other Rickettsiales,Aquarickettsiais undergoing positive selection, with Florida populations experiencing greater positive selection relative to the other Caribbean locations. This may be due toAquarickettsiaresponse to increased nutrient stress in Florida, as indicated by greaterin situreplication rates in these corals.Aquarickettsiadid 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,Aquarickettsiamust be horizontally transmitted via coral mucocytes, an unidentified secondary host, or a yet unexplored environmentally mediated mechanism. Importantly, the prevalence ofAquarickettsiainAc. cervicornisand high abundance in Florida populations suggests that disease mitigation efforts in the US and Caribbean should focus on preventing early infection via horizontal transmission.