It is largely unknown how living organisms—especially vertebrates—survive and thrive in the coldness, darkness and high pressures of the hadal zone. Here, we describe the unique morphology and genome of Pseudoliparis swirei—a recently described snailfish species living below a depth of 6,000 m in the Mariana Trench. Unlike closely related shallow sea species, P. swirei has transparent, unpigmented skin and scales, thin and incompletely ossified bones, an inflated stomach and a non-closed skull. Phylogenetic analyses show that P. swirei diverged from a close relative living near the sea surface about 20 million years ago and has abundant genetic diversity. Genomic analyses reveal that: (1) the bone Gla protein (bglap) gene has a frameshift mutation that may cause early termination of cartilage calcification; (2) cell membrane fluidity and transport protein activity in P. swirei may have been enhanced by changes in protein sequences and gene expansion; and (3) the stability of its proteins may have been increased by critical mutations in the trimethylamine N-oxide-synthesizing enzyme and hsp90 chaperone protein. Our results provide insights into the morphological, physiological and molecular evolution of hadal vertebrates.

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