Late Miocene threshold response of marine algae to carbon dioxide limitation

Coccolithophores are marine algae that use carbon for calcification and photosynthesis. The long-term adaptation of these and other marine algae to decreasing carbon dioxide levels during the Cenozoic era has resulted in modern algae capable of actively enhancing carbon dioxide at the site of photosynthesis. This enhancement occurs through the transport of dissolved bicarbonate (HCO3(-)) and with the help of enzymes whose expression can be modulated by variable aqueous carbon dioxide concentration, [CO2], in laboratory cultures. Coccolithophores preserve the geological history of this adaptation because the stable carbon and oxygen isotopic compositions of their calcite plates (coccoliths), which are preserved in the fossil record, are sensitive to active carbon uptake and transport by the cell. Here we use a model of cellular carbon fluxes and show that at low [CO2] the increased demand for HCO3(-) at the site of photosynthesis results in a diminished allocation of HCO3(-) to calcification, which is most pronounced in larger cells. This results in a large divergence between the carbon isotopic compositions of small versus large coccoliths only at low [CO2]. Our evaluation of the oxygen and carbon isotope record of size-separated fossil coccoliths reveals that this isotopic divergence first arose during the late Miocene to the earliest Pliocene epoch (about 7-5 million years ago). We interpret this to be a threshold response of the cells' carbon acquisition strategies to decreasing [CO2]. The documented coccolithophore response is synchronous with a global shift in terrestrial vegetation distribution between 8 and 5 Myr ago, which has been interpreted by some studies as a floral response to decreasing partial pressures of carbon dioxide () in the atmosphere. We infer a global decrease in carbon dioxide levels for this time interval that has not yet been identified in the sparse proxy record but is synchronous with global cooling and progressive glaciations.