Morphology and genome of a snailfish from the Mariana Trench provide insights into deep-sea adaptation

Kun Wang,Zhaoming Gao,Lisheng He,Yongzhi Yang,Yongxin Li,Xiujuan Shan,Qiang Qiu,Honghui Zeng,Xiangchao Gan ,Wenjie Xu,Chenguang Feng,Guichun Liu,Liandong Yang,Chenglong Zhu,Wuhan Xiao,Yang Dong,Wen Wang,Chang Liu,Suxiang Lu,Guoyong Yan,Kuang Hu,Yuan Yuan,Li Zhu,Xiangyu Pan,Yanjun Shen,Shunping He

doi:10.1038/s41559-019-0864-8

Abstract

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.

Highlights

It is largely unknown how living organisms—especially vertebrates—survive and thrive in the coldness, darkness and high pressures of the hadal zone
During a recent expedition in the Mariana Trench—the world’s deepest known ocean trench—a previously unknown snailfish was observed in situ at a depth of 7,415 m, and was identified as a new species, Pseudoliparis swirei[9]
Mariana hadal snailfish (MHS) specimens were caught at a depth of about seven kilometres at multiple locations in the Mariana Trench (Fig. 1a) using the deep-sea landers Tianya and Haijiao, operated from the RV Tan Suo Yi Hao (Fig. 1b–d, Supplementary Table 1 and Supplementary Note 1)

Summary

Introduction

It is largely unknown how living organisms—especially vertebrates—survive and thrive in the coldness, darkness and high pressures of the hadal zone. 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. The deepest areas of the ocean (that is, those between 6,000 and 11,000 m) are commonly referred to as the hadal zone, and represent ~1–2% of the global benthic area[1] They are among the most hostile environments on Earth, due to their high hydrostatic pressure, darkness, limited food resources, low temperatures and hypoxia[2]. During a recent expedition in the Mariana Trench—the world’s deepest known ocean trench—a previously unknown snailfish was observed in situ at a depth of 7,415 m, and was identified as a new species, Pseudoliparis swirei[9]. We present comparative morphological, genomic and transcriptomic analyses of P. swirei that provide insights into genetic changes associated with adaptation to the deep sea

Methods

Results

Conclusion