Specialised gut symbionts in deep-sea holothurian Chiridota hydrothermica support host nutrition and biogeochemical cycling in cold seep ecosystems

Abstract

Sea cucumbers are ecologically important deposit feeders that mediate organic material recycling in benthic ecosystems. In the deep sea, where the trophic structures differ markedly from those in the euphotic zone, the gut symbionts of sea cucumbers may function as essential mediators in nutrient transformation and biogeochemical cycling. However, the taxonomic composition and metabolic potentials of these gut symbionts remain poorly understood. In the present study, we performed comparative metagenomic analyses of the gut contents of a deep-sea sea cucumber Chiridota hydrothermica and adjacent sediments from the Haima cold seep in the South China Sea. In total, 145 metagenome-assembled genomes (MAGs) were reconstructed, representing a broad diversity across 35 prokaryotic phyla, with 10 gut-abundant, 64 sediment-abundant, and 71 shared MAGs. The gut symbionts of C. hydrothermica were characterised by high abundance of the Gammaproteobacteria, Desulfobacterota, and Bacteroidia, and they exhibited elevated abundance of genes for carbohydrate and amino acid metabolism. Members of Bacteroidia harboured extensive CAZyme repertoires involved in polysaccharide degradation, which were abundant in the gut symbionts. Additionally, genes associated with methane oxidation and sulphur cycling were enriched in specific MAGs in the sea cucumber guts. Our findings revealed taxonomically distinct and functionally specialised gut symbionts that underpin nutrient transformation and biogeochemical cycling in the deep-sea sea cucumber, highlighting potential microbial contributions to host ecological adaptation in cold seep ecosystems.

Keywords

Cold seep / Host nutrition / Biogeochemical cycling / Gut / Deep-sea adaptation

References

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Funding

Hong Kong University of Science and Technology

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