Unfolding the secrets of microbiome (Symbiodiniaceae and bacteria) in cold-water coral

Recent deep-ocean exploration has uncovered a variety of cold-water coral (CWC) ecosystems around the world ocean, but it remains unclear how microbiome is associated with these corals at a molecular levels. This study utilized metabarcoding, tissue section observation, and metatranscriptomes to investigate the microbiome (Symbiodiniaceae and bacteria) of CWC species (Narella versluysi, Heterogorgia uatumani, and Muriceides sp.) from depths ranging from 260 m to 370 m. Warm-water coral (WWC) species (Acropora pruinosa, Pocillopora damicornis, and Galaxea fascicularis) were used as control groups. Results revealed that CWC host diverse bacteria and Symbiodiniaceae cells were observed in endoderm of CWC tissues. Several new candidate bacterial phyla were found in both CWC and WWC, including Coralsanbacteria, Coralqiangbacteria, Coralgsqaceae, Coralgongineae, etc. Both the 16S rRNA gene sequencing and metatranscriptomes revealed that Actinobacteria and Proteobacteria were abundant bacterial phyla in CWC. At the gene transcription level, the CWC-associated Symbiodiniaceae community showed a low-level transcription of genes involved in photosynthesis, CO2 fixation, glycolysis, citric acid cycle, while bacteria associated with CWC exhibited a high-level transcription of genes for carbon fixation via the Wood-Lijungdahl pathway, short chain fatty acids production, nitrogen, and sulfur cycles. IMPORTANCE This study shed new light on the functions of both Symbiodiniaceae and bacteria in cold-water coral (CWC). The results demonstrated that Symbiodiniaceae can survive and actively transcribe genes in CWC, suggesting a possible symbiotic or parasitic relationship with the host. This study also revealed complete non-photosynthetic CO2 fixation pathway of bacteria in CWC, as well as their roles in short chain fatty acids production and assimilation of host-derived organic nitrogen and sulfur. These findings highlight the important role of bacteria in the carbon, nitrogen sulfur cycles in CWC, which were possibly crucial for CWC survival in in deep-water environments.