Whole genome sequencing of a snailfish from the Yap Trench (~7,000 m) clarifies the molecular mechanisms underlying adaptation to the deep sea.

Yinnan Mu,Guangming Shao,Ying Qiu,Xinhua Chen,Wanru Li,Qiong Shi,Ruoyu Liu,Jingqun Ao,Jia Li,Tianliang He,Chao Bian,Yuguang Wang,Gregory P Copenhaver

doi:10.1371/journal.pgen.1009530

Abstract

Hadal environments (depths below 6,000 m) are characterized by extremely high hydrostatic pressures, low temperatures, a scarce food supply, and little light. The evolutionary adaptations that allow vertebrates to survive in this extreme environment are poorly understood. Here, we constructed a high-quality reference genome for Yap hadal snailfish (YHS), which was captured at a depth of ~7,000 m in the Yap Trench. The final YHS genome assembly was 731.75 Mb, with a contig N50 of 0.75 Mb and a scaffold N50 of 1.26 Mb. We predicted 24,329 protein-coding genes in the YHS genome, and 24,265 of these genes were successfully functionally annotated. Phylogenetic analyses suggested that YHS diverged from a Mariana Trench snailfish approximately 0.92 million years ago. Many genes associated with DNA repair show evidence of positive selection and have expanded copy numbers in the YHS genome, possibly helping to maintain the integrity of DNA under increased hydrostatic pressure. The levels of trimethylamine N-oxide (TMAO), a potent protein stabilizer, are much higher in the muscles of YHS than in those of shallow-water fish. This difference is perhaps due to the five copies of the TMAO-generating enzyme flavin-containing monooxygenase-3 gene (fmo3) in the YHS genome and the abundance of trimethylamine (TMA)-generating bacteria in the YHS gut. Thus, the high TMAO content might help YHS adapt to high hydrostatic pressure by improving protein stability. Additionally, the evolutionary features of the YHS genes encoding sensory-related proteins are consistent with the scarce food supply and darkness in the hadal environments. These results clarify the molecular mechanisms underlying the adaptation of hadal organisms to the deep-sea environment and provide valuable genomic resources for in-depth investigations of hadal biology.

Highlights

The hadal zone (6,000–11,000 m deep) is composed mainly of deep trenches, and is usually characterized by extremely high hydrostatic pressures, low temperatures, a scarce food supply, a lack of light, and geographical isolation [1,2]
We constructed a high-quality reference genome for Yap hadal snailfish (YHS) captured at a depth of ~7,000 m in the Yap Trench, using long reads obtained by Pacific Biosciences Sequel sequencing
Comparative genomic analyses revealed that many genes associated with DNA repair show evidence of positive selection and have expanded copy numbers in the YHS genome, which potentially reflect the difficulty of maintaining DNA integrity under high hydrostatic pressure

Summary

Introduction

The hadal zone (6,000–11,000 m deep) is composed mainly of deep trenches, and is usually characterized by extremely high hydrostatic pressures, low temperatures, a scarce food supply, a lack of light, and geographical isolation [1,2]. The food resources in the hadal zone are mainly supplemented by surface-derived carrion falls, which implies that the food in the hadal zone is much more limited than that in shallower regions [1,5] These harsh living conditions form a unique deep ocean trench ecosystem with an endemic faunal community distinct from those in surrounding deep-sea environments [6]. Substitutions in lactate dehydrogenase in deep-sea fishes help the enzyme better tolerate high hydrostatic pressures [7] Another potential mechanism of pressure adaptation involves several small organic solutes, which are referred to as “pyrolites” [10,11]. At low temperatures, the DNA and RNA strand structures tend to tighten, which hinders interaction with enzymes involved in DNA replication, transcription, and translation and disrupts the transcription and translation processes [9]

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Discussion

Conclusion