Function and Development of Deep-sea Mussel Bacteriocytes Revealed by SnRNA-seq and Spatial Transcriptomics

The deep-sea chemosynthetic ecosystems are among one of the most unusual ecosystems on Earth, where most megafauna form close symbiotic associations with chemosynthetic microbes to obtain nutrition and shelter from the toxic environment. Despite the diverse forms of symbiotic organs in these deep-sea holobionts, the function and development of bacteriocytes, the host cells harboring symbionts, are still largely uncharacterized. Here, we have conducted the in situ decolonization assay and state-of-the-art single-nucleus and spatial transcriptomics to reveal the function and development of deep-sea mussel bacteriocytes. The bacteriocytes appear to optimize immune processes to facilitate recognition, engulfment, and elimination of endosymbionts. They also interact directly with them in carbohydrate and ammonia metabolism by exchanging metabolic intermediates via transporters such as SLC37A2 and RHBG-A. Bacteriocytes arise from three different proliferating cell types, and their successive development trajectory was delineated by multi-omics data and 3D reconstruction analyses. The molecular functions and the developmental processes of bacteriocytes were found to be guided by the same set of molluscan-conserved transcription factors and may be influenced by endosymbionts through sterol metabolism. The coordination in the functions and development of bacteriocytes and between the host and symbionts highlights the phenotypic plasticity of symbiotic cells, and underpins host-symbiont interdependence in adaptation to the deep sea.