Microbiome restructuring: dominant coral bacterium Endozoicomonas species display differential adaptive capabilities to environmental changes

Bacteria in the coral microbiome play a crucial role in determining coral health and fitness, and the coral host often restructures its microbiome composition in response to external factors. An important but often neglected factor determining this microbiome restructuring is the capacity of microbiome members to adapt to a new environment. To address this issue, we examined how the microbiome structure of Acropora muricata corals changed over 9 months following a reciprocal transplant experiment. Using a combination of metabarcoding, genomics, and comparative genomics approaches, we found that coral colonies separated by a small distance harbored different dominant Endozoicomonas related phylotypes belonging to two different species, including a novel species, Candidatus Endozoicomonas penghunesis 4G, whose chromosome level (complete) genome was also sequenced in this study. Furthermore, the two dominant Endozoicomonas species showed varied adaptation capabilities when coral colonies were transplanted in a new environment. The differential adaptation capabilities of dominant members of the microbiome can a) provide distinct advantages to coral hosts when subjected to changing environmental conditions and b) have positive implications for future reefs.

Similarities and Differences Between Two Deadly Caribbean Coral Diseases: White Plague and Stony Coral Tissue Loss Disease

For several decades, white plagues (WPDs: WPD-I, II and III) and more recently, stony coral tissue loss disease (SCTLD) have significantly impacted Caribbean corals. These diseases are often difficult to separate in the field as they produce similar gross signs. Here we aimed to compare what we know about WPD and SCTLD in terms of: (1) pathology, (2) etiology, and (3) epizootiology. We reviewed over 114 peer-reviewed publications from 1973 to 2021. Overall, WPD and SCTLD resemble each other macroscopically, mainly due to the rapid tissue loss they produce in their hosts, however, SCTLD has a more concise case definition. Multiple-coalescent lesions are often observed in colonies with SCTLD and rarely in WPD. A unique diagnostic sign of SCTLD is the presence of bleached circular areas when SCTLD lesions are first appearing in the colony. The paucity of histopathologic archives for WPDs for multiple species across geographies makes it impossible to tell if WPD is the same as SCTLD. Both diseases alter the coral microbiome. WPD is controversially regarded as a bacterial infection and more recently a viral infection, whereas for SCTLD the etiology has not been identified, but the putative pathogen, likely to be a virus, has not been confirmed yet. Most striking differences between WPD and SCTLD have been related to duration and phases of epizootic events and mortality rates. While both diseases may become highly prevalent on reefs, SCTLD seems to be more persistent even throughout years. Both transmit directly (contact) and horizontally (waterborne), but organism-mediated transmission is only proven for WPD-II. Given the differences and similarities between these diseases, more detailed information is needed for a better comparison. Specifically, it is important to focus on: (1) tagging colonies to look at disease progression and tissue mortality rates, (2) tracking the fate of the epizootic event by looking at initial coral species affected, the features of lesions and how they spread over colonies and to a wider range of hosts, (3) persistence across years, and (4) repetitive sampling to look at changes in the microbiome as the disease progresses. Our review shows that WPDs and SCTLD are the major causes of coral tissue loss recorded in the Caribbean.

Local versus site-level effects of algae on coral microbial communities

Microbes influence ecological processes, including the dynamics and health of macro-organisms and their interactions with other species. In coral reefs, microbes mediate negative effects of algae on corals when corals are in contact with algae. However, it is unknown whether these effects extend to larger spatial scales, such as at sites with high algal densities. We investigated how local algal contact and site-level macroalgal cover influenced coral microbial communities in a field study at two islands in French Polynesia, Mo'orea and Mangareva. At 5 sites at each island, we sampled prokaryotic microbial communities (microbiomes) associated with corals, macroalgae, turf algae and water, with coral samples taken from individuals that were isolated from or in contact with turf or macroalgae. Algal contact and macroalgal cover had antagonistic effects on coral microbiome alpha and beta diversity. Additionally, coral microbiomes shifted and became more similar to macroalgal microbiomes at sites with high macroalgal cover and with algal contact, although the microbial taxa that changed varied by island. Our results indicate that coral microbiomes can be affected by algae outside of the coral's immediate vicinity, and local- and site-level effects of algae can obscure each other's effects when both scales are not considered.

Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality

Beneficial microorganisms for corals (BMCs) ameliorate environmental stress, but whether they can prevent mortality and the underlying host response mechanisms remains elusive. Here, we conducted omics analyses on the coral Mussismilia hispida exposed to bleaching conditions in a long-term mesocosm experiment and inoculated with a selected BMC consortium or a saline solution placebo. All corals were affected by heat stress, but the observed “post-heat stress disorder” was mitigated by BMCs, signified by patterns of dimethylsulfoniopropionate degradation, lipid maintenance, and coral host transcriptional reprogramming of cellular restructuration, repair, stress protection, and immune genes, concomitant with a 40% survival rate increase and stable photosynthetic performance by the endosymbiotic algae. This study provides insights into the responses that underlie probiotic host manipulation. We demonstrate that BMCs trigger a dynamic microbiome restructuring process that instigates genetic and metabolic alterations in the coral host that eventually mitigate coral bleaching and mortality.

Host traits and evolution shape key coral-bacterial symbioses

The success of tropical scleractinian corals depends on their ability to establish symbioses with microbial partners. Host traits and evolution are known to shape the coral microbiome, but to what extent they affect its composition remains unclear. Here, by using twelve coral species representing the complex and robust clades, we show that functional traits and host evolutionary history explain 14% of the tissue and 13% of the skeletal microbiome composition, providing evidence that these predictors contribute to shaping the holobiont in terms of the presence and abundance of key bacterial species. Additionally, our study shows that the coral tissue and skeleton are dominated by rare bacteria and the skeleton can function as a microbial reservoir. Together, we provide novel insights into the processes driving coral-bacterial symbioses along with an improved understanding of the scleractinian tissue and skeleton microbiome.

Dispersal Limitation Expands the Diversity of Coral Microbiome Metacommunity in the South China Sea

The coral microbiome is one of the most complex microbial biospheres. However, the ecological processes shaping coral microbiome community assembly are not well understood. Here, we investigated the abundance, diversity, and community assembly mechanisms of coral-associated microbes from a highly diverse coral metacommunity in the South China Sea. Compared to seawater, the coral microbial metacommunity were defined by highly variable bacterial abundances among individual coral samples, high species evenness but not high species richness, high β-diversity, and a small core microbiome. We used variation partitioning analysis, neutral community model, and null model to disentangle the influences of different ecological processes in coral microbiome assembly. Measured physico-chemical parameters of the surrounding seawater and the spatial factor together explained very little of the variation in coral microbiome composition. Neutral processes only explained a minor component of the variation of coral microbial communities, suggesting a non-stochastic community assembly. Homogeneous and heterogeneous selection, but not dispersal, contributed greatly to the assembly of the coral microbiome. Such selection could be attributed to the within-host environments rather than the local environments. Our results demonstrated that dispersal limitation and host filtering contribute significantly to the assembly of discrete coral microbial regimes and expand the metacommunity diversity.

Comparison of Preservation and Extraction Methods on Five Taxonomically Disparate Coral Microbiomes

All animals are host to a multitude of microorganisms that are essential to the animal’s health. Host-associated microbes have been shown to defend against potential pathogens, provide essential nutrients, interact with the host’s immune system, and even regulate mood. However, it can be difficult to preserve and obtain nucleic acids from some host-associated microbiomes, making studying their microbial communities challenging. Corals are an example of this, in part due to their potentially remote, underwater locations, their thick surface mucopolysaccharide layer, and various inherent molecular inhibitors. This study examined three different preservatives (RNAlater, DNA/RNA Shield, and liquid nitrogen) and two extraction methods (the Qiagen PowerBiofilm kit and the Promega Maxwell RBC kit with modifications) to determine if there was an optimum combination for examining the coral microbiome. These methods were employed across taxonomically diverse coral species, including deep-sea/shallow, stony/soft, and zooxanthellate/azooxanthellate: Lophelia pertusa, Paragorgia johnsoni, Montastraea cavernosa, Porites astreoides, and Stephanocoenia intersepta. Although significant differences were found between preservative types and extraction methods, these differences were subtle, and varied in nature from coral species to coral species. Significant differences between coral species were far more profound than those detected between preservative or extraction method. We suggest that the preservative types presented here and extraction methods using a bead-beating step provide enough consistency to compare coral microbiomes across various studies, as long as subtle differences in microbial communities are attributed to dissimilar methodologies. Additionally, the inclusion of internal controls such as a mock community and extraction blanks can help provide context regarding data quality, improving downstream analyses.

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

Background The coral holobiont is comprised of a highly diverse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes and tied to ecosystem functioning, as it constitutes the direct interface between the coral host and the environment. The functional profile of microbial genes in the coral SML is underexplored and the use of shotgun metagenomics is relatively rare among coral microbiome studies. Here we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. Results The analysis was conducted using metagenomes and metagenome assemble genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctuating thermal regime and the more stable outer reefs . Our results showed that the microbial community structure is simultaneously selected by the host medium (i.e., coral SML versus water) and the local environment (i.e., inner reefs versus outer reefs), both at taxonomic and functional levels. The coral SML microbiome from inner reefs provides more gene functions that are involved in nutrient cycling (e.g., photosynthesis, phosphorus metabolism, sulfur assimilation) and that are related to higher levels of microbial activity, competition, and stress response, such as dimethylsulfoniopropionate (DMSP) breakdown. In contrast, the coral SML microbiome from outer reefs contained genes indicative of a carbohydrate-rich mucus composition found in corals exposed to less stressful temperatures and showed high proportions of microbial gene functions that play a potential role in coral disease, such as degradation of lignin-derived compounds and sulfur oxidation. Conclusion The fluctuating environment in the inner patch reefs of Bermuda could be driving a more beneficial coral SML microbiome; potentially increasing holobiont resilience to environmental changes and disease. Our results reveal microbial taxa and functions selected at reef scale in the coral SML microbiome that can leverage disease management, microbiome engineering, and microbial eco-evolutionary theories.

Shifting the microbiome of a coral holobiont and improving host physiology by inoculation with a potentially beneficial bacterial consortium

Background The coral microbiome plays a key role in host health by being involved in energy metabolism, nutrient cycling, and immune system formation. Inoculating coral with beneficial bacterial consortia may enhance the ability of this host to cope with complex and changing marine environments. In this study, the coral Pocillopora damicornis was inoculated with a beneficial microorganisms for corals (BMC) consortium to investigate how the coral host and its associated microbial community would respond. Results High-throughput 16S rRNA gene sequencing revealed no significant differences in bacterial community α-diversity. However, the bacterial community structure differed significantly between the BMC and placebo groups at the end of the experiment. Addition of the BMC consortium significantly increased the relative abundance of potentially beneficial bacteria, including the genera Mameliella and Endozoicomonas. Energy reserves and calcification rates of the coral host were also improved by the addition of the BMC consortium. Co-occurrence network analysis indicated that inoculation of coral with the exogenous BMC consortium improved the physiological status of the host by shifting the coral-associated microbial community structure. Conclusions Manipulating the coral-associated microbial community may enhance the physiology of coral in normal aquarium conditions (no stress applied), which may hypothetically contribute to resilience and resistance in this host.