Recent ocean acidification (OA) studies revealed that seawater [H+] rather than [CO2] or [HCO3-] regulate short-term responses in carbon fluxes of Emiliania huxleyi. Here, we investigated whether acclimation to altered carbonate chemistry modulates this regulation pattern and how the carbon supply for calcification is affected by carbonate chemistry. We acclimated E. huxleyi to present-day (ambient [CO2], [HCO3-], and pH) and OA conditions (high [CO2], ambient [HCO3-], low pH). To differentiate between the CO2 and pH/H+ effects, we also acclimated cells to carbonation (high [CO2] and [HCO3-], ambient pH) and acidification (ambient [CO2], low [HCO3-], and pH). Under these conditions, growth, production of particulate inorganic and organic carbon, as well as carbon and oxygen fluxes were measured. Under carbonation, photosynthesis and calcification were stimulated due to additional [HCO3-] uptake, whereas growth was unaffected. Such stimulatory effects are not apparent after short-term carbonation, indicating that cells adjusted their carbon acquisition during acclimation. Being driven by [HCO3-], these regulations can, however, not explain typical OA effects. Under acidification and OA, photosynthesis stayed constant, whereas calcification and growth decreased. Similar to the short-term responses toward high [H+], CO2 uptake significantly increased, but HCO3- uptake decreased. This antagonistic regulation in CO2 and HCO3- uptake can explain why photosynthesis, being able to use CO2 and HCO3-, often benefits from OA, whereas calcification, being mostly dependent on HCO3-, often decreases. We identified H+ as prime driver of coccolithophores' acclimation responses toward OA. Acidified conditions seem to put metabolic burdens on the cells that result in decreased growth.