Single-cell perspectives on the function and development of deep-sea mussel bacteriocytes

Symbiosis is known to be a major force driving the adaptation and evolution of multicellular organisms. The symbiotic cells and organs, on the meantime, directly provide the mutualist services to the host as the source of phenotypic complexity and outcome of development plasticity. The investigations on the formation and development of symbiotic cells and organs however still remain a challenge in both model and non-model holobionts. Here, by constructing the high-resolution single-cell expression atlas of gill tissue, we have thoroughly surveyed the population census and function atlas of bacteriocytes in deep-sea mussel. Results showed that the bacteriocytes have markedly reshaped its metabolism and are highly coordinated with the endosymbionts in the metabolism of sterol, carbohydrate and ammonia. The immune process of bacterioytes is also robustly adjusted to facilitate the recognition, engulfment, elimination and transcellular transport of endosymbionts. Noticeably, we recognized that the molecular function of bacteriocytes could be guided synergistically by co-option of several conserved transcription factors of the regulatory networks. Moreover, these conserved transcription factors were also responsible for the differentiation and maturation of bacteriocyte lineages. Our results have for the first time revealed the coordination in the function and development of deep-sea mussel symbiotic cells, which was mediated by an ancestral and intrinsic toolkit that conserved across mollusk and could be influenced by symbionts. The coordination while greatly improved our knowledge on how deep-sea mussel thrive in the extreme environment of deep-sea, also highlighted a promising roadmap in revealing the formation and development of symbiotic cells and organs in all holobionts.