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

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 musselGigantidas platifronsfrom the South China Sea methane seeps (1100m depth) using single-nucleus RNA sequencing (snRNA-seq) and whole-mountin situhybridisation. 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 ofin situtransplanted 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.