Reef-building corals are well regarded not only for their obligate association with endosymbiotic algae, but also with prokaryotic symbionts, the specificity of which remains elusive. To identify the central microbial symbionts of corals, their specificity across species and conservation over geographic regions, we sequenced partial SSU ribosomal RNA genes of Bacteria and Archaea from the common corals Stylophora pistillata and Pocillopora verrucosa across 28 reefs within seven major geographical regions. We demonstrate that both corals harbor Endozoicomonas bacteria as their prevalent symbiont. Importantly, catalyzed reporter deposition–fluorescence in situ hybridization (CARD–FISH) with Endozoicomonas-specific probes confirmed their residence as large aggregations deep within coral tissues. Using fine-scale genotyping techniques and single-cell genomics, we demonstrate that P. verrucosa harbors the same Endozoicomonas, whereas S. pistillata associates with geographically distinct genotypes. This specificity may be shaped by the different reproductive strategies of the hosts, potentially uncovering a pattern of symbiont selection that is linked to life history. Spawning corals such as P. verrucosa acquire prokaryotes from the environment. In contrast, brooding corals such as S. pistillata release symbiont-packed planula larvae, which may explain a strong regional signature in their microbiome. Our work contributes to the factors underlying microbiome specificity and adds detail to coral holobiont functioning.

Endozoicomonas bacteria are globally distributed and often abundantly associated with diverse marine hosts including reef-building corals, yet their function remains unknown. In this study we generated novel Endozoicomonas genomes from single cells and metagenomes obtained directly from the corals Stylophora pistillata, Pocillopora verrucosa, and Acropora humilis. We then compared these culture-independent genomes to existing genomes of bacterial isolates acquired from a sponge, sea slug, and coral to examine the functional landscape of this enigmatic genus. Sequencing and analysis of single cells and metagenomes resulted in four novel genomes with 60–76% and 81–90% genome completeness, respectively. These data also confirmed that Endozoicomonas genomes are large and are not streamlined for an obligate endosymbiotic lifestyle, implying that they have free-living stages. All genomes show an enrichment of genes associated with carbon sugar transport and utilization and protein secretion, potentially indicating that Endozoicomonas contribute to the cycling of carbohydrates and the provision of proteins to their respective hosts. Importantly, besides these commonalities, the genomes showed evidence for differential functional specificity and diversification, including genes for the production of amino acids. Given this metabolic diversity of Endozoicomonas we propose that different genotypes play disparate roles and have diversified in concert with their hosts.

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal-microbial relationships have historically been explored in single host-symbiont systems. However, new explorations into the diversity of microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more diverse microbiome. The potential for microbiomes to influence the health, physiology, behavior and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment. This review explores the nature of marine animal-microbiome relationships and interactions, and possible factors that may shift associations from symbiotic to dissociated states. I present a brief review of current microbiome research and opportunities, using examples of select marine animals that span diverse phyla within the Animalia, including systems that are more and less developed for symbiosis research, including two represented in my own research program. Lastly, I consider challenges and emerging solutions for moving these and other study systems into a more detailed understanding of host-microbiome interactions within a changing ocean.

Summary: Coral‐associated microorganisms are thought to play a fundamental role in the health and ecology of corals, but understanding of specific coral–microbial interactions are lacking. In order to create a framework to examine coral–microbial specificity, we integrated and phylogenetically compared 21,100 SSU rRNA gene Sanger‐produced sequences from bacteria and archaea associated with corals from previous studies, and accompanying host, location and publication metadata, to produce the Coral Microbiome Database. From this database, we identified 39 described and candidate phyla of Bacteria and two Archaea phyla associated with corals, demonstrating that corals are one of the most phylogenetically diverse animal microbiomes. Secondly, this new phylogenetic resource shows that certain microorganisms are indeed specific to corals, including evolutionary distinct hosts. Specifically, we identified 2–37 putative monophyletic, coral‐specific sequence clusters within bacterial genera associated with the greatest number of coral species ( Vibrio , Endozoicomonas and Ruegeria ) as well as functionally relevant microbial taxa (“ Candidatus Amoebophilus ”, “Candidatus Nitrosopumilus” and under recognized cyanobacteria). This phylogenetic resource provides a framework for more targeted studies of corals and their specific microbial associates, which is timely given the escalated need to understand the role of the coral microbiome and its adaptability to changing ocean and reef conditions.

The pulmonary system is a common site for bacterial infections in cetaceans, but very little is known about their respiratory microbiome. We used a small, unmanned hexacopter to collect exhaled breath condensate (blow) from two geographically distinct populations of apparently healthy humpback whales (Megaptera novaeangliae), sampled in the Massachusetts coastal waters off Cape Cod (n = 17) and coastal waters around Vancouver Island (n = 9). Bacterial and archaeal small-subunit rRNA genes were amplified and sequenced from blow samples, including many of sparse volume, as well as seawater and other controls, to characterize the associated microbial community. The blow microbiomes were distinct from the seawater microbiomes and included 25 phylogenetically diverse bacteria common to all sampled whales. This core assemblage comprised on average 36% of the microbiome, making it one of the more consistent animal microbiomes studied to date. The closest phylogenetic relatives of 20 of these core microbes were previously detected in marine mammals, suggesting that this core microbiome assemblage is specialized for marine mammals and may indicate a healthy, noninfected pulmonary system. Pathogen screening was conducted on the microbiomes at the genus level, which showed that all blow and few seawater microbiomes contained relatives of bacterial pathogens; no known cetacean respiratory pathogens were detected in the blow. Overall, the discovery of a shared large core microbiome in humpback whales is an important advancement for health and disease monitoring of this species and of other large whales. IMPORTANCE The conservation and management of large whales rely in part upon health monitoring of individuals and populations, and methods generally necessitate invasive sampling. Here, we used a small, unmanned hexacopter drone to noninvasively fly above humpback whales from two populations, capture their exhaled breath (blow), and examine the associated microbiome. In the first extensive examination of the large-whale blow microbiome, we present surprising results about the discovery of a large core microbiome that was shared across individual whales from geographically separated populations in two ocean basins. We suggest that this core microbiome, in addition to other microbiome characteristics, could be a useful feature for health monitoring of large whales worldwide.

This study demonstrates that coral tissue or mucus habitats structure the microbiome of corals and that separation of these habitats facilitates identification of consistent microbial associates. Using this approach, we demonstrated that sequences related to “ Candidatus Amoebophilus,” recognized intracellular symbionts of amoebae, were highly associated with the tissues of Caribbean corals and possibly endosymbionts of a protistan host within corals, adding a further degree of intricacy to coral holobiont symbioses. Examining specific habitats within complex hosts such as corals is useful for targeting important microbial associations that may otherwise be masked by the sheer microbial diversity associated with all host habitats.