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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 era1 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 cultures2,3. 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 atmosphere4,5,6. We infer a global decrease in carbon dioxide levels for this time interval that has not yet been identified in the sparse proxy record7 but is synchronous with global cooling and progressive glaciations8,9.

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Figure 1: HCO3 allocation to the chloroplast and coccolith vesicle inferred from εcoccolith measured in culture.
Figure 2: Divergence of vital effects in coccoliths.
Figure 3: Evolution of vital effects in coccoliths, C4 photosynthesis and 16 Myr ago.


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We thank L. Abrevaya and A. Mendez for laboratory assistance, and K. Lawrence for access to unpublished data. This work used samples provided by the (Integrated) Ocean Drilling Program (IODP). The IODP is sponsored by the US National Science Foundation and participating countries under management of the IODP Management International, Inc. Funding for this research was provided by European Research Council grant UE-09-ERC-2009-STG-240222-PACE (H.M.S.) and a DuPont Young Professor Award to H.M.S.

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C.T.B. and H.M.S. designed the study and wrote the paper. C.T.B. separated coccoliths and performed stable isotope, light microscope and scanning electron microscope analyses. H.M.S. designed and ran the model.

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Correspondence to Clara T. Bolton or Heather M. Stoll.

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The authors declare no competing financial interests.

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Bolton, C., Stoll, H. Late Miocene threshold response of marine algae to carbon dioxide limitation. Nature 500, 558–562 (2013).

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