GUARDIANS OF THE CELL: COCCOSPHERE PREVENTS OPPORTUNISTIC BACTERIA ATTACK IN HEAVY CALCIFYING COCCOLITHOPHORE

Abstract

Coccolithophores are responsible for 40-60% of marine calcium carbonate production. This occurs through the biomineralization of extracellular calcium carbonate plates that encase the cell in a structure called the coccosphere. Despite its central role in ocean biogeochemistry, the function of coccolithophore calcification remains unresolved. One hypothesis is that the coccosphere acts as a physical shield, deterring predators and microbes. While its protective role has been investigated against grazers and viruses, its function in bacterial defense remains untested. Here, we investigate the interaction between heavily calcified Coccolithus braarudii and the bacterial pathogen Phaeobacter inhibens, known for its lethal Jekyll and Hyde relationship with the bloom-forming Gephyrocapsa huxleyi. We find that in C. braarudii, no P. inhibens pathogenicity is observed--unless the algae are decalcified. Upon decalcification, the relationship with P. inhibens becomes pathogenic, leading to algal cell death. Mortality of decalcified cells is specific to interactions with P. inhibens and is attachment-mediated: no toxicity is observed when cells are exposed to P. inhibens supernatant or to growth-inhibiting concentrations of indole-3-acetic acid-- identified in the P. inhibens-G. huxleyi system. Attachment requirement is further supported by scanning electron microscopy, which reveals extensive bacterial colonization on decalcified but not on calcified C. braarudii with P. inhibens. These findings provide the first experimental evidence that the coccosphere acts as a physical barrier against bacterial attack, underscoring its defensive role in coccolithophores.