Azooxanthellate scleractinian corals, which lack symbiotic dinoflagellates, occur from shallow waters to deep-sea environments. In deep-sea benthic ecosystems, they serve as foundation species and are considered highly vulnerable to environmental disturbances. However, their genomic diversities and the genetic basis of their fully heterotrophic lifestyles remain poorly understood. In this study, the genome of a deep-sea solitary coral, Polymyces sp., was sequenced. Integrated with the published genomes of the deep-sea colonial coral Desmophyllum pertusum and two shallow-water azooxanthellate corals Dendrophyllia cribrosa and Catalaphyllia jardinei, the adaptive mechanisms of fully heterotrophic lifestyles were investigated. For genomic diversity comparisons, Illumina short-read data for deep-sea (Polymyces sp., D. pertusum, and Madrepora oculata) and zooxanthellate corals (Porites australiensis) were generated. The results indicated that reduced genomic diversity was found in azooxanthellate scleractinians compared with zooxanthellate relatives. Signatures of recent inbreeding were detected in Polymyces sp. and D. cribrosa, potentially contributing to their low recent effective population sizes and the endangered status of D. cribrosa. Lineage-specific gene losses affecting circadian rhythm, immunity, and autophagy were also detected in the above two species, suggesting overly streamlined energy-saving trade-offs that may impair functional flexibility. Interestingly, the cosmopolitan deep-sea D. pertusum retained complete light-sensing and circadian clock complements, whereas deep-sea Polymyces sp. with evidence of recent inbreeding showed substantial reductions, suggesting that photosensitivity and biological clocks may remain important for ecological success even in the deep-sea environment. Convergent adaptations were supported by concordant patterns of gene-family contraction and positive selection shared among the four azooxanthellate scleractinians. The contractions were concentrated in functions related to photosensitivity, lipid metabolism, and mitochondrial processes, consistent with life in dark and oligotrophic habitats, whereas significant signatures of positive selection were detected on vesicle transport-related genes, highlighting the key roles of vesicle-mediated endosomal pathways in a photosymbiosis-free lifestyle. This study provides a genomic perspective on the evolution of heterotrophic strategies in scleractinian corals and highlights conservation concerns for nonsymbiotic corals under accelerating global stressors.
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