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

Abstract

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.

Phenotypic Plasticity of Symbiotic Organ Highlight Deep-sea Mussel as Model Species in Monitoring Exploitation of Deep-sea Methane Hydrate

“…Moreover, the differential expression of the sterol-related signaling pathway under methane deprivation might be a cascade reaction triggered by the shortage of symbiont-deprived sterol intermediates 37 . In support of this speculation, data from the single-cell transcriptome analysis also suggested that the methanotrophic symbionts could influence the differentiation and maturation processes of bacteriocytes via the sterol-related signaling pathway 43 . It is also noticeable that majority of animal hosts have formed coordinated sterol metabolism with their symbionts, highlighting the possible role of sterol-related signaling pathway in the phenotypic plasticity of symbiotic cells and organs across different holobionts.…”

“…Therefore, phenotypic changes in symbiotic cells and organs can occur frequently in part or in whole for deep-sea mussels regarding to the intensity of environmental change and serve as key indicators of deep-sea mining or other anthropogenic activities. Besides, the deep-sea mussel could survive even much longer than one year in natural condition since our experimental condition is much harsh 31,43 . While the phenotypic changes of the digestion system remain unexplored, the long-term survival of deep-sea mussels under methane deprivation might also endow them with transgenerational effects, allowing for a permanent transition from chemoautotrophy (a symbiotic association with thiotrophs) or chemoheterotrophy (a symbiotic association with methanotrophs) to strict heterotrophy (filter-feeding).…”

Symbioses from Cold Seeps

“…Recently, it was demonstrated that bacteriocytes could retrieve fructose-6-phosphate (F6P) directly from methanotrophic symbionts by sugar phosphate exchanger genes and convert it into glucose-6-phosphate (G6P), fructose-1,6-bisphosphate (F-1,6-BP) and glyceraldehyde-3-phosphate (G6P) before redistributing them back to both the host and symbionts as supplements of gluconeogenesis and the tricarboxylic acid cycle (TCA cycle). A direct supply of ammonia from the host to symbionts via ammonium transporters was also reported (Chen et al 2022). The bioconversion and exchange of sugar phosphate and ammonia between the host and symbionts provided an efficient and direct way to coordinate the metabolism of both partners, which greatly promoted the efficiency and profits of symbiosis.…”