Abstract

Cold seeps and hydrothermal vents are deep-sea reducing environments that are characterized by lacking oxygen and photosynthesis-derived nutrients. Most animals acquire nutrition in cold seeps or hydrothermal vents by maintaining epi- or endosymbiotic relationship with chemoautotrophic microorganisms. Although several seep- and vent-dwelling animals hosting symbiotic microbes have been well-studied, the genomic basis of adaptation to deep-sea reducing environment in nonsymbiotic animals is still lacking. Here, we report a high-quality genome of Chiridota heheva Pawson & Vance, 2004, which thrives by extracting organic components from sediment detritus and suspended material, as a reference for nonsymbiotic animal’s adaptation to deep-sea reducing environments. The expansion of the aerolysin-like protein family in C. heheva compared with other echinoderms might be involved in the disintegration of microbes during digestion. Moreover, several hypoxia-related genes (Pyruvate Kinase M2, PKM2; Phospholysine Phosphohistidine Inorganic Pyrophosphate Phosphatase, LHPP; Poly(A)-specific Ribonuclease Subunit PAN2, PAN2; and Ribosomal RNA Processing 9, RRP9) were subject to positive selection in the genome of C. heheva, which contributes to their adaptation to hypoxic environments.

Highlights

  • Cold seeps and hydrothermal vents are deep-sea reducing environments that are characterized by lacking oxygen and photosynthesis-derived nutrients

  • Chemosynthetic microbes oxidize the reduced chemicals contained in the hydrocarbon fluids to produce energy and fix carbon into organic matter, which supports a large amount of invertebrates, including tubeworms, mussels, clams, and gastropods[15]

  • Most of these macrobenthos depend on the epi- or endosymbiotic relationships with chemoautotrophic microorganisms for nutrition[14,16,17]

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Summary

Results and discussion

Characterization and genome assembly of C. heheva. The sequenced sample was collected at a depth of 1385 meters using manned submersible Shenhaiyongshi from the Haima cold seep in the South China Sea (16° 73.228′ N, 110° 46.143′ E) (Fig. 1). To determine whether Hox genes contribute to morphological divergence in Holothuroidea, we identified Hox gene clusters and their evolutionary sister complex, the ParaHox gene cluster, in the genomes of C. heheva and 6 other echinoderms (Supplementary Fig. 3). PKM2 increases glycolysis and decreases oxygen consumption by promoting transactivation of HIF-1 target genes through directly interacting with the HIF-1α subunit under hypoxic conditions[54] This suggests that animals living in deep-sea chemosynthetic environments might adapt to hypoxic conditions through reprogramming glucose metabolism. LHPP gene was subjected to positive selection in both C. heheva and cetaceans This indicates a possible convergent evolution, in which echinoderms and mammals utilize similar strategies to cope with hypoxic challenges

Methods
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