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Fig 1.

Collection and morphology of Yap hadal snailfish and its genomic characteristics.

(A) Bathymetric map of the Yap Trench. The red dot indicates the location at which the two hadal snailfishes were caught by the Chinese manned submersible Jiaolong. The bathymetric map was obtained from GEBCO Compilation Group (2020) GEBCO 2020 Grid (doi:10.5285/a29c5465-b138-234d-e053-6c86abc040b9). (B) Yap hadal snailfish (YHS) in situ at 6,903 m (above) and after capture (below). (C) Distribution of TE families across the YHS genome: DNA transposons (DNA), long interspersed nuclear elements (LINEs), long terminal repeats (LTRs), short interspersed nuclear elements (SINEs), and unknown TEs (unknown). (D) Venn diagram showing shared and unique gene families across YHS, Mariana hadal snailfish, Tanaka’s snailfish, and zebrafish.

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Table 1.

Statistics of the genome assembly and annotation of Yap hadal snailfish.

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Fig 2.

Coalescent species tree and divergence time estimation for Yap hadal snailfish and 20 other teleost species.

Human served as the outgroup species. The purple rectangle bar at each node indicates the 95% confidence interval. The numbers at nodes represent estimated divergence times (Mya), and the numbers on branches indicate the event of gene family expansion (red) and contraction (blue). YHS: Yap hadal snailfish, MHS: Mariana hadal snailfish.

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Fig 3.

Genomic indications of enhanced DNA repair mechanisms in the Yap hadal snailfish (YHS).

(A) Gene ontology enrichment of the positively selected genes from YHS (level 4). CC, cellular component, MF, molecular function, BP, biological process. (B, C) Partial alignment of the (B) RAD52 and (C) RAD9A amino acid sequences from various representative teleosts and human. Amino acids unique to two hadal snailfishes (YHS and Mariana hadal snailfish) are highlighted in red; positions within each sequence are given above. (D) A maximum-likelihood tree showing RAD51 and RAD51 paralog genes (RAD51b, RAD51c, XRCC2, XRCC3, and DMC1). The leaf-node colors correspond to the species given in panels (B) and (C).

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Fig 4.

Potential mechanism of TMAO-mediated protein stabilization in Yap hadal snailfish.

(A) Muscle TMAO contents (mmol/kg wet mass) in three teleosts. (B) Arrangement of the TMAO-generating enzyme fmo3 genes in the genomes of Yap hadal snailfish (YHS), Mariana hadal snailfish, Tanaka’s snailfish, large yellow croaker, and zebrafish. (C) Relative expression of fmo3 genes in the liver, muscle, intestine, skin, and stomach of YHS. Gene expression was quantified as fragments per kilobase of transcript per million fragments mapped (FPKM) values. (D) Bacterial communities in the YHS gut identified using the Silva database. (E) Proposed TMAO biosynthesis pathway in the YHS. Through this pathway, both the gut microbiota and five copies of fmo3 help to maintain a high TMAO levels and thus improve protein stability to ameliorate the destabilizing effects of hydrostatic pressure.

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Fig 5.

Genetic features of the unique sensory systems of Yap hadal snailfish.

(A) Evolution and synteny of taste genes across several representative teleosts. The reference gene positions were based on the zebrafish genome. The white pentagons indicate lost genes. Tas2r: taste receptor type 2, pkd2l1: polycystic kidney disease 2-like 1. (B) Numbers of functional genes or pseudogenes encoding δ group olfactory receptors in various fish species. (C) Amino acid residues at the nine critical nine sites in rhodopsin across representative fish species and λmax values of rhodopsin in different fish species. YHS: Yap hadal snailfish, MHS: Mariana hadal snailfish, Sia: Sinocyclocheilus anshuiensis, Sig: Sinocyclocheilus grahami, Sir: Sinocyclocheilus rhinocerous.

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