Cold seeps in the deep sea harbor various animals that have adapted to utilize seepage chemicals with the aid of chemosynthetic microbes that serve as primary producers. Corals are among the animals that live near seep habitats and yet, there is a lack of evidence that corals gain benefits and/or incur costs from cold seeps. Here, we focused on Callogorgia delta and Paramuricea sp. type B3 that live near and far from visual signs of currently active seepage at five sites in the deep Gulf of Mexico. We tested whether these corals rely on chemosynthetically‐derived food in seep habitats and how the proximity to cold seeps may influence; (i) coral colony traits (i.e., health status, growth rate, regrowth after sampling, and branch loss) and associated epifauna, (ii) associated microbiome, and (iii) host transcriptomes. Stable isotope data showed that many coral colonies utilized chemosynthetically derived food, but the feeding strategy differed by coral species. The microbiome composition of C. delta, unlike Paramuricea sp., varied significantly between seep and non‐seep colonies and both coral species were associated with various sulfur‐oxidizing bacteria (SUP05). Interestingly, the relative abundances of SUP05 varied among seep and non‐seep colonies and were strongly correlated with carbon and nitrogen stable isotope values. In contrast, the proximity to cold seeps did not have a measurable effect on gene expression, colony traits, or associated epifauna in coral species. Our work provides the first evidence that some corals may gain benefits from living near cold seeps with apparently limited costs to the colonies. Cold seeps provide not only hard substrate but also food to cold‐water corals. Furthermore, restructuring of the microbiome communities (particularly SUP05) is likely the key adaptive process to aid corals in utilizing seepage‐derived carbon. This highlights that those deep‐sea corals may upregulate particular microbial symbiont communities to cope with environmental gradients.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/gcb.16447

Capacity of deep‐sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization

Coral-associated microbiomes vary greatly between coral colonies and sampling locations with functional consequences on the coral host. However, the full extent of variability across the ranges of most coral species remains unknown, especially in octocorals and species from mesophotic and deep-sea habitats. Here we characterized the microbiomes of four octocoral species from mesophotic and deep-sea habitats in the northern Gulf of Mexico, Muricea pendula, Swiftia exserta, Callogorgia delta, and Paramuricea biscaya using 16S metabarcoding. We tested for microbiome differentiation between and within species, examining the influence of the coral’s genotype and environmental factors that vary with depth (53-2224 m) and geographic location (over 680 m). Coral microbiomes were often dominated by a single amplicon sequence variant – ASV (>50% relative abundance) whose abundance varied across the range of the host coral. These included corallicolid apicomplexans, Endozoicomonas, members of the Mollicutes, and the BD1-7 clade of Spongiibacteraceae. Coral species, depth, and geographic location significantly affected microbial community composition, richness, and evenness, as well as the abundance of individual microbes. Differences in bottom temperature and surface primary productivity could explain part of the variation associated with depth and geographic location, respectively. However the coral genotype was confounded with depth so its effect could not be dissected. Altogether, this work demonstrates that the microbiomes of corals vary substantially across their ranges in ways that may have functional consequences, identifies important ecological drivers in mesophotic and deep-sea corals, and can inform restoration efforts.

https://www.biorxiv.org/content/biorxiv/early/2023/07/05/2023.07.05.547877.full.pdf

A seascape approach to the microbial biogeography of mesophotic and deep-sea octocorals

Abstract Background Coral-associated microbiomes vary greatly between colonies and localities with functional consequences on the host. However, the full extent of variability across the ranges of most coral species remains unknown, especially for corals living in deep waters which span greater ranges. Here, we characterized the microbiomes of four octocoral species from mesophotic and bathyal deep-sea habitats in the northern Gulf of Mexico, Muricea pendula, Swiftia exserta, Callogorgia delta, and Paramuricea biscaya, using 16S rRNA gene metabarcoding. We sampled extensively across their ranges to test for microbiome differentiation between and within species, examining the influence of environmental factors that vary with depth (53–2224 m) and geographic location (over 680 m) as well as the host coral’s genotype using RAD-sequencing. Results Coral microbiomes were often dominated by amplicon sequence variants whose abundances varied across their hosts’ ranges, including symbiotic taxa: corallicolids, Endozoicomonas , members of the Mollicutes , and the BD1-7 clade. Coral species, depth, and geographic location significantly affected diversity, microbial community composition, and the relative abundance of individual microbes. Depth was the strongest environmental factor determining microbiome structure within species, which influenced the abundance of most dominant symbiotic taxa. Differences in host genotype, bottom temperature, and surface primary productivity could explain a significant part of the microbiome variation associated with depth and geographic location. Conclusions Altogether, this work demonstrates that the microbiomes of corals in deep waters vary substantially across their ranges in accordance with depth and other environmental conditions. It reveals that the influence of depth on the ecology of mesophotic and deep-sea corals extends to its effects on their microbiomes which may have functional consequences. This work also identifies the distributions of microbes including potential parasites which can be used to inform restoration plans in response to the Deepwater Horizon oil spill. 

pdf/coral-microbiomes-are-structured-by-environmental-gradients-2wqhx2as5b.pdf

Coral microbiomes are structured by environmental gradients in deep waters

Abstract Background The Gorgonian coral, Eunicella singularis , is one of the main components of Mediterranean marine animal forests, whose canopies play a key role in Mediterranean sublittoral ecosystems due to their capacity to provide shelter, food, and nursery ground to several species. Like other gorgonian species, E. singularis faces environmental threats with potential repercussions on the associated biodiversity. This photophilic octocoral, spanning the Western Mediterranean, Adriatic, and Aegean Seas at depths of 10-70m, engages in symbiosis with Symbiodiniaceae dinoflagellates, thereby influencing their resilience in nutrient-poor habitats. However, mesophotic populations (∼60m depth) are characterized by very low Symbiodiniaceae density, prompting questions regarding metabolic adaptations. The associations of corals with specific bacteria that differ from those in the surrounding seawater suggest a role in host health and physiology. In particular, in mesophotic colonies, bacteria may perform activities that Symbiodinium typically carries out in shallow colonies. Here, we applied metagenomics techniques to analyze the changes in the microbiome of Eunicella singularis with depth, analyzing DNA samples from shallow (12m) and mesophotic (57m) colonies in the Northwestern Mediterranean Sea. Results High-coverage metagenomes (ca. 80 Gb per sample) were generated from E. singularis colony samples. We observed significant changes in the relative abundance of prokaryotic and microbial eukaryotic symbionts with depth. Mesophotic samples exhibited higher levels of symbiotic prokaryotes, dominated by Endozoicomonas and Bermanella , whereas shallow samples were enriched with the symbiotic dinoflagellate Symbiodiniaceae . The metabolic potential of the microbiome also varied with depth. The shallow microbiome showed a prevalence of photosynthesis and carbon fixation pathways. In turn, the mesophotic microbiome exhibited a higher abundance of metabolic functions related to vitamin biosynthesis, energy metabolism, especially carbon metabolism, as well as pathways associated with carbohydrates, amino acids, and cofactors. Conclusions Our results indicate that the structure and metabolic function of the microbiome of Eunicella singularis change with depth. In the absence of symbiotic dinoflagellates, associated bacteria seem to use different sources of carbon, in addition to cycling nutrients and vitamins, which could influence coral health. These findings gain significance in the context of global change, as shifts in oceanic conditions may affect the coral microbiome. 

Microbiome composition and function vary with depth in the Mediterranean gorgonian Eunicella singularis

In addition to abundant animal communities, corals from all ocean depths support diverse microbial associates that are important to coral health. While some of these microbes have been classified taxonomically, understanding the metabolic potential of coral-associated bacteria and how they interact with their coral hosts is limited by a lack of genomic data. One example is Mycoplasma and other members of the class Mollicutes which are widespread coral associates. Here we investigated the association between two novel members of the class Mollicutes and the deep-sea octocoral Callogorgia delta. We screened C. delta, a closely related species C. americana, sediment, and water for mollicutes using 16S metabarcoding. One ASV was found in most colonies screened (99/108) and often dominated the microbiome (up to 99%). Another ASV was detected at lower abundance and prevalence in these corals. Both were absent in all water and were absent or rare in the sediment. We sequenced metagenomes and metatranscriptomes to assemble and annotate genomes and propose the names Ca. Oceanoplasma callogorgiae and Ca. Thalassoplasma callogorgiae. The genomes were small, revealed a reliance on the arginine dihydrolase pathway for ATP production, and contained CRISPR-Cas systems with extensive arrays. CARD-FISH microscopy unveiled an abundant bacterium in the mesoglea which is likely to be Ca. O. callogorgiae. These novel mollicutes cluster with others from diverse invertebrate hosts. Altogether, this work describes the association of these novel mollicutes in C. delta, provides insight into widespread coral associates, and identifies a novel clade of marine mollicutes whose diversity remains largely undiscovered.

/pdf/the-deep-sea-coral-callogorgia-delta-associates-with-3p5sar5f.pdf

The deep-sea coral, Callogorgia delta, associates with bacteria belonging to a novel marine branch of the Mollicutes

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The deep-sea coral, Callogorgia delta, associates with bacteria belonging to a novel marine branch of the Mollicutes