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

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

Research output: Contribution to journalArticle

Abstract

Hydrothermal vents and methane seeps are extreme deep-sea ecosystems that support dense populations of specialized macro- benthos 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.

Original languageEnglish (US)
Article number0121
JournalNature Ecology and Evolution
Volume1
Issue number5
DOIs
StatePublished - Apr 3 2017

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Ecology

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  • Cite this

    Sun, J., Zhang, Y., Xu, T., Zhang, Y., Mu, H., Zhang, Y., Lan, Y., Fields, C. J., Hui, J. H. L., Zhang, W., Li, R., Nong, W., Cheung, F. K. M., Qiu, J. W., & Qian, P. Y. (2017). Adaptation to deep-sea chemosynthetic environments as revealed by mussel genomes. Nature Ecology and Evolution, 1(5), [0121]. https://doi.org/10.1038/s41559-017-0121