Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; Laboratory for Marine Biology and Biotechnology, Qingdao Marine Science and Technology Center, Laoshan Laboratory, Qingdao, China; Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China; Department of Ocean Science, Hong Kong University of Science and Technology, Hong Kong, China
Kai He
Key Laboratory of Conservation and Application in Biodiversity of South China, School of Life Sciences, Guangzhou University, Guangzhou, China
Huan Zhang
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Quanyong Zhang
State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Japan
Lei Cao
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Jing Li
South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Li Zhou
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Chao Lian
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Minxiao Wang
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China
Kai Chen
State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, Japan
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China; Department of Ocean Science, Hong Kong University of Science and Technology, Hong Kong, China
Chaolun Li
Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China; South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China; University of Chinese Academy of Sciences, Beijing, China
Bathymodioline mussels dominate deep-sea methane seep and hydrothermal vent habitats and obtain nutrients and energy primarily through chemosynthetic endosymbiotic bacteria in the bacteriocytes of their gill. However, the molecular mechanisms that orchestrate mussel host–symbiont interactions remain unclear. Here, we constructed a comprehensive cell atlas of the gill in the mussel Gigantidas platifrons from the South China Sea methane seeps (1100 m depth) using single-nucleus RNA-sequencing (snRNA-seq) and whole-mount in situ hybridisation. We identified 13 types of cells, including three previously unknown ones, and uncovered unknown tissue heterogeneity. Every cell type has a designated function in supporting the gill’s structure and function, creating an optimal environment for chemosynthesis, and effectively acquiring nutrients from the endosymbiotic bacteria. Analysis of snRNA-seq of in situ transplanted mussels clearly showed the shifts in cell state in response to environmental oscillations. Our findings provide insight into the principles of host–symbiont interaction and the bivalves' environmental adaption mechanisms.