Phagocytosis of exogenous bacteria by gill epithelial cells in the deep-sea symbiotic mussel Bathymodiolus japonicus

Abstract

Animals that live in nutrient-poor environments, such as the deep sea, often establish intracellular symbiosis with beneficial bacteria that provide the host with nutrients that are usually inaccessible to them. The deep-sea mussel Bathymodiolus japonicus relies on nutrients from the methane-oxidizing bacteria harboured in epithelial gill cells called bacteriocytes. These symbionts are specific to the host and transmitted horizontally, being acquired from the environment by each generation. Morphological studies in mussels have reported that the host gill cells acquire the symbionts via phagocytosis, a process that facilitates the engulfment and digestion of exogenous microorganisms. However, gill cell phagocytosis has not been well studied, and whether mussels discriminate between the symbionts and other bacteria in the phagocytic process remains unknown. Herein, we aimed to investigate the phagocytic ability of gill cells involved in the acquisition of symbionts by exposing the mussel to several types of bacteria. The gill cells engulfed exogenous bacteria from the environment indiscriminately. These bacteria were preferentially eliminated through intracellular digestion using enzymes; however, most symbionts were retained in the bacteriocytes without digestion. Our findings suggest that regulation of the phagocytic process after engulfment is a key mechanism for the selection of symbionts for establishing intracellular symbiosis.