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

Deep-sea chemosynthetic ecosystems are among 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 conducted an in situ decolonization assay and state-of-the-art single-nucleus and spatial transcriptomic analyses to reveal the function and development of deep-sea mussel bacteriocytes. Bacteriocytes appear to optimize immune processes to facilitate the recognition, engulfment, and elimination of endosymbionts. They also interact directly with endosymbionts in carbohydrate and ammonia metabolism by exchanging metabolic intermediates via transporters such as SLC37A2 and RHBG-A. Bacteriocytes arise from three different proliferation cell types, and their successive development trajectories were delineated using multi-omics data and 3D reconstruction analyses. The molecular functions and developmental processes of bacteriocytes are 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.