Molecular mechanisms, metabolic remodeling, and energy reallocation underlying calcification in the coccolithophore...

Coccolithophores play a dual role in the marine carbon cycle, serving as CO₂ sinks through photosynthesis while simultaneously emitting CO₂ via calcification, resulting in uncertainty regarding their net carbon sequestration potential. In addition, their calcite coccoliths (CaCO₃) can increase the carbon export efficiency by functioning as ballasts for organic matter. Although biogeochemically significant, the molecular mechanisms governing calcification and associated metabolic adaptations in coccolithophores remain poorly characterized, impeding accurate predictions of their responses to climate change. Through comparative multiomics analyses of calcified (RCC1266) and noncalcified (PML B92/11) Gephyrocapsa huxleyi strains, as well as chemically induced decalcified and recalcified states, we screened several ion transport genes, which potentially facilitate Ca²⁺ and HCO₃ ^- uptake/transport coupled with H⁺ extrusion during calcification in the calcified strain, along with their associated proteins, including signal molecules and chaperones. Furthermore, an energy-intensive process was observed in calcifying cells, and this process was principally sustained by enhanced photosynthetic efficiency, supplemented by glucose accumulation as an energy reserve and COX6B translational upregulation, providing nocturnal energy. Notably, calcifying cells employed an energy conservation strategy characterized by transcriptional downregulation yet translational maintenance of photosynthesis and carbon metabolism genes while simultaneously upregulating protein biosynthesis and trafficking pathways to probably meet calcification demands, a process potentially facilitated by increased glutamine biosynthesis. Through multiomic technology, our findings provide insights into the molecular adaptations in the calcified coccolithophorid cells, revealing critical physiological trade-offs, carbon metabolism, and energy allocation that can inform predictions of their acclimation capacity under changing oceanic conditions.