Deciphering deep-sea chemosynthetic symbiosis by single-nucleus RNA- sequencing

Author:

Wang Hao123,He Kai4,Zhang Huan1,Zhang Quanyong5,Cao Lei1,Li Jing16,Zhong Zhaoshan1,Chen Hao1,Zhou Li1,Lian Chao1,Wang Minxiao1,Chen Kai5,Qian Pei-Yuan23,Li Chaolun167

Affiliation:

1. Center of Deep-Sea Research, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

2. Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Nansha, Guangzhou, China

3. Department of Ocean Science, Hong Kong University of Science and Technology, Hong Kong S.A.R, China

4. Key Laboratory of Conservation and Application in Biodiversity of South China, School of Life Sciences, Guangzhou University, Guangzhou, Guangdong 510006, China

5. State Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming, China

6. South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, China

7. University of Chinese Academy of Sciences, Beijing, China

Abstract

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 (1100m 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, 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 principles of host-symbiont interaction and the bivalves’ environmental adaption mechanisms.

Publisher

eLife Sciences Publications, Ltd

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