Physiology regulates the relationship between coccosphere geometry and growth-phase in coccolithophores

Coccolithophores are an abundant phytoplankton group that exhibit remarkable diversity in their biology, ecology, and calcitic exoskeletons (coccospheres). Their extensive fossil record is testament to their important biogeochemical role and is a valuable archive of biotic responses to environmental change stretching back over 200 million years. However, to realise the potential of this archive requires an understanding of the physiological processes that underpin coccosphere architecture. Using culturing experiments on four modern coccolithophore species (Calcidiscus leptoporus, Calcidiscus quadriperforatus, Helicosphaera carteri and Coccolithus braarudii) from three long-lived families, we investigate how coccosphere architecture responds to shifts from exponential (rapid cell division) to stationary (slowed cell division) growth phases as cell physiology reacts to nutrient depletion. These experiments reveal statistical differences in cell size and the number of coccoliths per cell between these two growth phases, specifically that cells in exponential-phase growth are typically smaller with fewer coccoliths, whereas cells experiencing growth-limiting nutrient depletion have larger coccosphere sizes and greater numbers of coccoliths per cell. Although the exact numbers are species-specific, these growthphase shifts in coccosphere geometry demonstrate that the core physiological responses of cells to nutrient depletion results in increased cell sizes and coccoliths per cell across four different coccolithophore families (Calcidiscaceae, Coccolithaceae, Isochrysidaceae, Helicosphaeraceae), a representative diversity of this phytoplankton group. Building on this, direct comparison of coccosphere geometries in modern and fossil coccolithophores enables a proxy for growth phase to be developed that allows growth responses to environmental change to be investigated throughout their evolutionary history. Our data also shows that changes in growth rate and coccoliths per cell associated with growth-phase shifts can substantially alter cellular calcite production. Coccosphere geometry is therefore a valuable tool for accessing growth information in the fossil record that provides unprecedented insights into the biotic responses of species to environmental change and its potential biogeochemical consequences