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Calcifying marine phytoplankton - coccolithophores - are some of the most successful yet enigmatic organisms in the ocean, and are at risk from global change. In order to better understand how they will be affected we need to know 'why' coccolithophores calcify. Here we review coccolithophorid evolutionary history, cell biology, and insights from recent experiments to provide a critical assessment of the costs and benefits of calcification. We conclude that calcification has high energy demands, and that coccolithophores might have calcified initially to reduce grazing pressure, but that additional benefits such as protection from photo-damage and viral-bacterial attack further explain their high diversity and broad spectrum ecology. The cost-versusbenefit of these traits is illustrated by novel ecosystem modeling, although conclusive observations are still limited. In the future ocean, the trade-off between changing ecological and physiological costs of calcification and their benefits will ultimately decide how this important group is affected by ocean acidification and global warming.

Rubisco, the most abundant enzyme on the Earth and responsible for all photosynthetic carbon fixation, is often thought of as a highly conserved and sluggish enzyme. Yet, different algal Rubiscos demonstrate a range of kinetic properties hinting at a history of evolution and adaptation. Here, we show that algal Rubisco has indeed evolved adaptively during ancient and distinct geological periods. Using DNA sequences of extant marine algae of the red and Chromista lineage, we define positive selection within the large subunit of Rubisco, encoded by rbcL, to occur basal to the radiation of modern marine groups. This signal of positive selection appears to be responding to changing intracellular concentrations of carbon dioxide (CO2) triggered by physiological adaptations to declining atmospheric CO2. Within the ecologically important Haptophyta (including coccolithophores) and Bacillariophyta (diatoms), positive selection occurred consistently during periods of falling Phanerozoic CO2 and suggests emergence of carbon-concentrating mechanisms. During the Proterozoic, a strong signal of positive selection after secondary endosymbiosis occurs at the origin of the Chromista lineage (approx. 1.1 Ga), with further positive selection events until 0.41 Ga, implying a significant and continuous decrease in atmospheric CO2 encompassing the Cryogenian Snowball Earth events. We surmise that positive selection in Rubisco has been caused by declines in atmospheric CO2 and hence acts as a proxy for ancient atmospheric CO2.

An increase in whole ocean alkalinity during glacial periods could account, in part, for the drawdown of atmospheric CO2 into the ocean. Such an increase was inevitable due to the near elimination of shelf area for the burial of coral reef alkalinity. We present evidence, based on downcore measurements of benthic foraminiferal B/Ca and Mg/Ca from a core in the Weddell Sea, that the deep ocean carbonate ion concentration, [CO32-], was elevated by similar to 25 mu mol/kg during each glacial period of the last 800 kyr. The heterogeneity of the preservation histories in the different ocean basins reflects control of the carbonate chemistry of the deep glacial ocean in the Atlantic and Pacific by the changing ventilation and chemistry of Weddell Sea waters. These waters are more corrosive than interglacial northern sourced waters but not as undersaturated as interglacial southern sourced waters. Our inferred increase in whole ocean alkalinity can be reconciled with reconstructions of glacial saturation horizon depth and the carbonate budget if carbonate burial rates also increased above the saturation horizon as a result of enhanced pelagic calcification. The Weddell records display low [CO32-] during deglaciations and peak interglacial warmth, coincident with maxima in percent CaCO3 in the Atlantic and Pacific oceans. Should the burial rate of alkalinity in the more alkaline glacial deep waters outstrip the rate of alkalinity supply, then pelagic carbonate production by the coccolithophores at the end of the glacial maximum could drive a decrease in ocean [CO32-] and act to trigger the deglacial rise in pCO(2).

Coccolithophores play a critical role in the balance between the chemistry of the atmosphere, ocean and sediments. Over geological time, amongst the population of coccolithophore species present, particular bloom forming species have risen to dominance. Every species of coccolithophore initiates the growth of calcite liths with a protococcolith ring consisting of calcite crystals with alternating vertically or radially oriented c-axes, the V/R model (Young et al., 1992). But the modern bloom species, Emiliania huxleyi, appears to exploit the faster propagation of radial calcite crystals which grow largely with obtuse kink sites parallel to the c-axis (Paquette and Reeder, 1995) to produce liths consisting almost entirely of radial calcite. Cations larger than calcium are preferentially incorporated into the less spatially restricted obtuse kink sites of calcite with a radially oriented c-axis, and cations smaller than calcium are preferentially incorporated into the acute sites of calcite with a vertically oriented c-axis. We hypothesis that the different orientations of crystal growth may also have implications for the stable isotopic composition of the calcite liths. Sediment records from the global ocean reveal an inverse relationship between coccolith fraction Mg/Ca and Sr/Ca during the last 1 Myr with a strong resonance of bloom species production at 100 and 400 kyr periods at times of low eccentricity. We propose that these trace metal and isotopic records demonstrate a relationship between orbital eccentricity and the production of bloom species growing radial calcite liths in the Pleistocene ocean (Rickaby et al.), perhaps as a result of the inverse relationship between growing season length and insolation under conditions of high eccentricity. We shall explore, with a geological perspective, the complex interplay between atmospheric chemistry, ocean saturation and the evolution of coccolithophores and their geochemistry.