Cell proliferation and apoptosis in gill filaments of the lucinid Codakia orbiculata (Montagu, 1808) (Mollusca: Bivalvia) during bacterial decolonization and recolonization

The shallow-water bivalve Codakia orbiculata which harbors gill-endosymbiotic sulfur-oxidizing γ-proteobacteria can lose and acquire its endosymbionts throughout its life. Long-term starvation and recolonization experiments led to changes in the organization of cells in the lateral zone of gill filaments. This plasticity is linked to the presence or absence of gill-endosymbionts. Herein, we propose that this reorganization can be explained by three hypotheses: (a) a variation in the number of bacteriocytes and granule cells due to proliferation or apoptosis processes, (b) a variation of the volume of these two cell types without modification in the number, and (c) a combination of both number and cell volume variation. To test these hypotheses, we analyzed cell reorganization in terms of proliferation and apoptosis in adults submitted to starvation and returned to the field using catalyzed reporter deposition fluorescence in situ hybridization, immunohistochemistry, and structural analyses. We observed that cell and tissue reorganization in gills filaments is due to a variation in cell relative abundance that maybe associated with a variation in cell apparent volume and depends on the environment. In fact, bacteriocytes mostly multiply in freshly collected and newly recolonized individuals, and excess bacteriocytes are eliminated in later recolonization stages. We highlight that host tissue regeneration in gill filaments of this symbiotic bivalve can occur by both replication of existing cells and division of undifferentiated cells localized in tissular bridges, which might be a tissue-specific multipotent stem cell zone.