Greater functional diversity and redundancy of coral endolithic microbiomes align with lower coral bleaching susceptibility

Abstract

The skeleton of reef-building coral harbors diverse microbial communities that could compensate for metabolic deficiencies caused by the loss of algal endosymbionts, i.e., coral bleaching. However, it is unknown to what extent endolith taxonomic diversity and functional potential might contribute to thermal resilience. Here we exposed Goniastrea edwardsi and Porites lutea, two common reef‐building corals from the central Red Sea to a 17-day long heat stress. Using hyperspectral imaging, marker gene/metagenomic sequencing, and NanoSIMS, we characterized their endolithic microbiomes together with 15N and 13C assimilation of two skeletal compartments: the endolithic band directly below the coral tissue and the deep skeleton. The bleaching-resistant G. edwardsi was associated with endolithic microbiomes of greater functional diversity and redundancy that exhibited lower N and C assimilation than endoliths in the bleaching-sensitive P. lutea. We propose that the lower endolithic primary productivity in G. edwardsi can be attributed to the dominance of chemolithotrophs. Lower primary production within the skeleton may prevent unbalanced nutrient fluxes to coral tissues under heat stress, thereby preserving nutrient-limiting conditions characteristic of a stable coral-algal symbiosis. Our findings link coral endolithic microbiome structure and function to bleaching susceptibility, providing new avenues for understanding and eventually mitigating reef loss.

Genomic view of the diversity and functional role of archaea and bacteria in the skeleton of the reef-building corals Porites lutea and Isopora palifera

“…But we did recover MAGs belonging to the archaeal class Nitrososphaeria and a few bacterial classes. Further, we identified a similar MAG community composition, although with significantly more diversity of MAGs recovered in our study compared to a recent study using a genome-centric approach on coral skeleton [ 36 ]. In light of these comparisons, we provide an exhaustive collection of skeletal dominated coral-associated bacterial and archaeal MAGs.…”

“…These studies are the only shallow-depth genome-centric research conducted to date on the coral skeleton, with a combination of FISH-nanoSIMS (Fluorescence in situ hybridization-nanoscale secondary ion mass spectrometry) and the acetylene reduction assay to confirm the dinitrogen-fixing ability of dominant anaerobic phototrophs. A recent study used a combination of metabarcoding and gene- and genome-centric metagenomics to shed light on the role of the endolithic microbiome in coral bleaching susceptibility [ 36 ]. The limited insights into the broader functional potential of coral skeletal microbiomes hamper our ability to identify key roles of the skeleton microbiota within the coral holobiont.…”

Deoxygenation lowers the thermal threshold of coral bleaching

“…A key aspect still missing is the contribution of other coral holobiont members to deoxygenation. For instance, associated microbes may be consuming large amounts of O 2 or shifting to a community of anaerobes, both of which could alter the overall O 2 budget of the coral holobiont 86 – 88 . Further, high microbial O 2 consumption associated with excessive algae production on coral reefs can lead to deoxygenation of the reef and consequential changes in the microbial and benthic communities 10 , 89 .…”

Millennia‐old coral holobiont DNA provides insight into future adaptive trajectories

“…Of the 103 bacterial genomes used as a “search space” in this study, a total of 10 had reads assigned from at least one ancient sample. These bacterial genomes corresponded mainly to bacterial populations associated with coral skeletons (Cárdenas et al, 2022). Mapping largely occurred in moderate to highly conserved gene regions shared across members of the same phylum (Figure S5) and indicating the presence of representatives of the phyla Bacteroidota, Desulfobacterota, Myxococcota, Proteobacteria and Spirochaetota in ancient samples.…”