Three-Dimensional Molecular Cartography of the Caribbean Reef-Building Coral Orbicella faveolata

Abstract

All organisms host a diversity of associated viruses, bacteria, and protists, collectively defined as the holobiont. While scientific advancements have enhanced the understanding of the functional roles played by various components of the holobiont, there is a growing need to integrate multiple types of molecular data into spatially and temporally resolved frameworks. To that end, we mapped 16S and 18S rDNA metabarcoding, metatranscriptomics, and metabolomic data onto three-dimensional reconstructions of coral colonies to examine microbial diversity, microbial gene expression, and biochemistry on two colonies of the ecologically important, reef-building coral, Orbicella faveolata and their competitors (i.e., adjacent organisms interacting with the corals: fleshy algae, turf algae, hydrozoans, and other corals). Overall, no statistically significant spatial patterns were observed among the samples for any of the data types; instead, strong signatures of the macroorganismal hosts (e.g., coral, algae, hydrozoa) were detected, in the microbiome, the transcriptome, and the metabolome. The 16S rDNA analysis demonstrated higher abundance of Firmicutes in the coral microbiome than in its competitors. A single bacterial amplicon sequence variant from the genus Clostridium was found exclusively in all O. faveolata samples. In contrast to microbial taxa, a portion of the functionally annotated bacterial RNA transcripts (6.86%) and metabolites (1.95%) were ubiquitous in all coral and competitor samples. Machine learning analysis of microbial transcripts revealed elevated T7-like cyanophage-encoded photosystem II transcripts in O. faveolata samples, while sequences involved in bacterial cell division were elevated in turf algal and interface samples. Similar analysis of metabolites revealed that bacterial-produced antimicrobial and antifungal compounds were highly enriched in coral samples. This study provides insight into the spatial and biological patterning of the coral microbiome, transcriptome, and metabolome.

Stony coral tissue loss disease: a review of emergence, impacts, etiology, diagnostics, and intervention

“…Advancement in untargeted metabolomics-based strategies offers an opportunity to connect cellular pathways with biological mechanisms, which is critical in unravelling the biological roles of metabolites in cellular physiology. Recent studies have demonstrated the applicability of metabolomics to evaluate physiological state and identify diagnostic biomarkers in Caribbean corals (Lohr et al, 2019;Roach et al, 2020;Little et al, 2021;Roach et al, 2021).…”

Advances in coral immunity ‘omics in response to disease outbreaks

“…We know from previous studies that coral genotypes have unique metabolomes, and that fragments of the same genotype have conserved metabolomes, highlighting the importance of knowing the genotype prior to investigation (Lohr et al, 2019). Visualization of spatial variation in 'omics data can further enable delineation of source of variation (Little et al, 2021). Together, multi-genotype experiments that use multiomics approaches will enable the development of a knowledge base to stratify corals in terms of disease resilience and holobiont composition to enable biomarker evaluation, and linkage of specific pathways in disease (Muller et al, 2018;Miller et al, 2019).…”

Microorganisms and dissolved metabolites distinguish Florida's Coral Reef habitats

“…Studies have documented relationships between reef microbial composition and reef parameters, including hard coral cover ( 26 , 27 ), temperature ( 28 , 29 ), chlorophyll ( 28 ), organic carbon ( 29 ), biogeography ( 27 , 30 ), and reef protection ( 31 ). To date, most investigations study either metabolites or microbes in isolation ( 16 , 19 , 22 ), though studies are increasingly combining techniques ( 32 , 33 ). A direct comparison of reef water metabolites and microorganisms is needed to inform the individual or collective value of these factors within reef habitats.…”