3D structural analysis of bacteriocytes in a deep-sea mussel Gigantidas platifrons with methanotrophic symbionts

Deep-sea mussels inhabit extreme environments through symbiosis with chemosynthetic bacteria, yet the three-dimensional (3D) ultrastructure of their bacteriocytes —the fundamental symbiotic units —remains elusive. This study employed advanced volume electron microscopy (vEM) to generate high-resolution, 3D models of bacteriocytes, revealing insights into the structural basis of stable symbiosis. We identified two distinct methanotrophic bacterial (MOB) morphotypes within the bacteriocytes: MOB^hd (high-density granule content) and MOB^ld (low-density granule content). MOB^hd, located in the apical region, undergoes lysis for nutrient release, while MOB^ld, situated in the interior, proliferates to maintain the symbiont population. Comparative analyses between gill and non-gill bacteriocytes revealed differential patterns of symbiont management, with gill bacteriocytes exhibiting more organized MOB distribution and orderly lysis. The 3D model unveiled a novel channel membrane system, potentially enhancing intracellular symbiont connectivity and facilitating distinct micro-niche occupation within the host cell. This organized structure maintains stable symbiosis, particularly in gill tissues. These findings advance our understanding of cellular mechanisms in symbiosis and adaptive strategies in extreme deep-sea environments.