Cooperation between bacteriocytes and endosymbionts drives function and development of symbiotic cells in mussel holobionts

Abstract

Symbiosis drives the adaptation and evolution in multicellular organisms. Modeling the function and development of symbiotic cells/organs in holobionts is yet challenging. Here, we surveyed the molecular function and developmental trajectory of bacteriocyte lineage in non-model deep-sea mussels by constructing a high-resolution single-cell expression atlas of gill tissue. We show that mussel bacteriocytes optimized immune genes to facilitate recognition, engulfment, and elimination of endosymbionts, and interacted with them intimately in sterol, carbohydrate, and ammonia metabolism. Additionally, the bacteriocytes could arise from three different stem cells as well as bacteriocytes themselves. In particular, we showed that the molecular functions and developmental process of bacteriocytes were guided by the same set of regulatory networks and dynamically altered regarding to symbiont abundance via sterol-related signaling. The coordination in the functions and development of bacteriocytes and between the host and symbionts underlies the interdependency of symbiosis, and drives the deep-sea adaptation of mussels.

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

“…In addition, the newly formed bacteriocytes of adult mussels also lose microvilli after being colonized by the symbionts of adjacent bacteriocytes (Wentrup et al, 2014). In our single-cell transcriptome study, we showed the participation of the sterol-related signaling pathway in the differentiation and maturation processes of mussel bacteriocytes (Chen et al, 2023). It is also noteworthy that the symbionts may control the function and development of host symbiotic organs in other symbiotic associations (Coon et al, 2017; Heath-Heckman et al, 2016; Nyholm and Mcfall-Ngai, 2021).…”