Genome sequencing of deep-sea hydrothermal vent snails reveals adaptions to extreme environments.

Xiang Zeng,Zongze Shao,Inge Seim,Lingfeng Meng,Nanxi Liu,Shanshan Liu,Guangyi Fan,Liping Wang,Xin Liu,Zenghua Shao,Yaolei Zhang,Jianwei Chen,Jie Bai,Congyan Wang,Yue Song,Haorong Lu,Xiaoteng Fu

doi:10.1093/gigascience/giaa139

Abstract

BackgroundThe scaly-foot snail (Chrysomallon squamiferum) is highly adapted to deep-sea hydrothermal vents and has drawn much interest since its discovery. However, the limited information on its genome has impeded further related research and understanding of its adaptation to deep-sea hydrothermal vents.FindingsHere, we report the whole-genome sequencing and assembly of the scaly-foot snail and another snail (Gigantopelta aegis), which inhabits similar environments. Using Oxford Nanopore Technology, 10X Genomics, and Hi-C technologies, we obtained a chromosome-level genome of C. squamiferum with an N50 size of 20.71 Mb. By constructing a phylogenetic tree, we found that these 2 deep-sea snails evolved independently of other snails. Their divergence from each other occurred ∼66.3 million years ago. Comparative genomic analysis showed that different snails have diverse genome sizes and repeat contents. Deep-sea snails have more DNA transposons and long terminal repeats but fewer long interspersed nuclear elements than other snails. Gene family analysis revealed that deep-sea snails experienced stronger selective pressures than freshwater snails, and gene families related to the nervous system, immune system, metabolism, DNA stability, antioxidation, and biomineralization were significantly expanded in scaly-foot snails. We also found 251 H-2 Class II histocompatibility antigen, A-U α chain-like (H2-Aal) genes, which exist uniquely in the Gigantopelta aegis genome. This finding is important for investigating the evolution of major histocompatibility complex (MHC) genes.ConclusionOur study provides new insights into deep-sea snail genomes and valuable resources for further studies.

Highlights

The scaly-foot snail (Chrysomallon squamiferum) is highly adapted to deep-sea hydrothermal vents and has drawn much interest since its discovery
We identified expanded gene families that maintain the stability of nucleic acids and proteins, such as heat shock protein 90 (Hsp90; 13 copies in C. squamiferum, Fig. 4a), which protects proteins against heat stress [35]; the single-stranded DNAbinding proteins, encoded by single-stranded DNA-binding protein (SSB) genes (19 copies in C. squamiferum, and 1 copy in other species, Fig. 4a), which are required for DNA replication, recombination, and repair processes [36]; and catalase (CAT, 6 copies C. squamiferum; Fig. 4c), which is critical in the response against oxidative stress [37]
Based on the chromosomescale genome assembly analyses of the scaly-foot snail (C. squamiferum) and deep-sea snail (G. aegis), which both belong to the Peltospiridae family from chemosynthetic ecosystems, our results provide insight into the possible evolution and adaptation mechanisms of hydrothermal vent animals

Summary

Background

The discovery of deep-sea hydrothermal vents in the late 1970s expanded our knowledge of the extent of life on Earth [1]. To explore the evolutionary rate of single-copy orthologous genes, we calculated the synonymous substitution rate (Ka) and nonsynonymous substitution rate (Ks) values of 1,324 singlecopy orthologous genes shared by the 2 deep-sea snails, 1 shallow-water limpet (Lottia gigantea), and 2 freshwater snails (B. glabrata and P. canaliculata) using Codeml in the PAML package (PAML, RRID:SCR 014932) [23] (Fig. 2c, Supplementary Fig. S3 and Table S15). Nervous system Using CAFE (CAFE, RRID:SCR 005983) [24] (see details in Methods), we identified 2 significantly (P < 0.01) expanded gene families in the 2 deep-sea snail genomes compared to the freshwater snails and shallow-water limpet. HTR4 (5hydroxytryptamine receptor 4) had 12 copies in C. squamiferum and 18 copies in G. aegis, while only 1 copy was found in the other snail species (Fig. 3c) The expansions of these gene families displayed tandem duplications (Supplementary Fig. S4). Vertebrate positions in G. aegis is useful for the study of immune system evolution

Discussion

Findings

Methods