Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes

Jin Sun,Wenyan Nong,Weipeng Zhang,Ting Xu,Pei-Yuan Qian,Yi Lan,Jian-Wen Qiu,Huawei Mu,Jerome Ho Lam Hui,Christopher J Fields,Fiona Ka Man Cheung,Yang Zhang,Runsheng Li,Yu Zhang,Yanjie Zhang

doi:10.1038/s41559-017-0121

Abstract

Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macrobenthos such as mussels. But the lack of genome information hinders the understanding of the adaptation of these animals to such inhospitable environments. Here we report the genomes of a deep-sea vent/seep mussel (Bathymodiolus platifrons) and a shallow-water mussel (Modiolus philippinarum). Phylogenetic analysis shows that these mussel species diverged approximately 110.4 million years ago. Many gene families, especially those for stabilizing protein structures and removing toxic substances from cells, are highly expanded in B. platifrons, indicating adaptation to extreme environmental conditions. The innate immune system of B. platifrons is considerably more complex than that of other lophotrochozoan species, including M. philippinarum, with substantial expansion and high expression levels of gene families that are related to immune recognition, endocytosis and caspase-mediated apoptosis in the gill, revealing presumed genetic adaptation of the deep-sea mussel to the presence of its chemoautotrophic endosymbionts. A follow-up metaproteomic analysis of the gill of B. platifrons shows methanotrophy, assimilatory sulfate reduction and ammonia metabolic pathways in the symbionts, providing energy and nutrients, which allow the host to thrive. Our study of the genomic composition allowing symbiosis in extremophile molluscs gives wider insights into the mechanisms of symbiosis in other organisms such as deep-sea tubeworms and giant clams.

Highlights

Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macrobenthos such as mussels
We sequenced the genomes of both B. platifrons Hashimoto and Okutani, 1994 and M. philippinarum (Hanley, 1843) in the family Mytilidae using a whole-genome shotgun approach and compared their features (Supplementary Note 1)
Using the lophotrochozoan tree as a reference, the time of divergence between B. platifrons and M. philippinarum was estimated to be around 110.4 million years ago (Ma), with a 95% confidence interval of 52.4–209.7 Ma (Fig. 2b), which is close to the upper age limit of deep-sea symbiotic mussels (102 Ma) previously estimated using five genes[14]

Summary

Introduction

Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macrobenthos such as mussels. Results and discussion We sequenced the genomes of both B. platifrons Hashimoto and Okutani, 1994 (a deep-sea mussel, Fig. 1a) and M. philippinarum (Hanley, 1843) (a shallow-water mussel, Fig. 1b) in the family Mytilidae using a whole-genome shotgun approach and compared their features (Supplementary Note 1). The deep-sea and shallow-water mussel genome contained 96.3% and 93.7% complete and partial universal single-copy metazoan orthologous genes, respectively, indicating the completeness of the assembly and gene models (Supplementary Note 6).

Results

Conclusion