The origin of carbon isotope vital effects in coccolith calcite

Calcite microfossils are widely used to study climate and oceanography in Earth’s geological past. Coccoliths, readily preserved calcite plates produced by a group of single-celled surface-ocean dwelling algae called coccolithophores, have formed a significant fraction of marine sediments since the Late Triassic. However, unlike the shells of foraminifera, their zooplankton counterparts, coccoliths remain underused in palaeo-reconstructions. Precipitated in an intracellular chemical and isotopic microenvironment, coccolith calcite exhibits large and enigmatic departures from the isotopic composition of abiogenic calcite, known as vital effects. Here we show that the calcification to carbon fixation ratio determines whether coccolith calcite is isotopically heavier or lighter than abiogenic calcite, and that the size of the deviation is determined by the degree of carbon utilization. We discuss the theoretical potential for, and current limitations of, coccolith-based CO2 paleobarometry, that may eventually facilitate use of the ubiquitous and geologically extensive sedimentary archive

Calcification response of a key phytoplankton family to millennial-scale environmental change

Coccolithophores are single-celled photosynthesizing marine algae, responsible for half of the calcification in the surface ocean, and exert a strong influence on the distribution of carbon among global reservoirs, and thus Earth’s climate. Calcification in the surface ocean decreases the buffering capacity of seawater for CO2, whilst photosynthetic carbon fixation has the opposite effect. Experiments in culture have suggested that coccolithophore calcification decreases under high CO2 concentrations ([CO2(aq)]) constituting a negative feedback. However, the extent to which these results are representative of natural populations, and of the response over more than a few hundred generations is unclear. Here we describe and apply a novel rationale for size-normalizing the mass of the calcite plates produced by the most abundant family of coccolithophores, the Noëlaerhabdaceae. On average, ancient populations subjected to coupled gradual increases in [CO2(aq)] and temperature over a few million generations in a natural environment become relatively more highly calcified, implying a positive climatic feedback. We hypothesize that this is the result of selection manifest in natural populations over millennial timescales, so has necessarily eluded laboratory experiments.HLOM was funded by PhD studentship NE/I019522/1 in association with UKOARP. REMR acknowledges NERC grant NE/H017119/1 and ERC grant SP2-GA-2008-200915. LB is grateful for financial support from EU Seventh Framework program Past4Future and from the Agence Nationale de la Recherche under project ANR-12-B06-0007 (CALHIS). PF was funded by Marie-Curie Reintegration grant (PERG-GA-2010-272134 - MILLEVARIABILI), funded by the EU PNRA 2013/AZ2.06 and GEOSMART, funded by the Italian National Antarctic Research Programme

Carbon dioxide and coccolithophore physiology in ancient oceans

Coccolithophores form an important and dynamically evolving component of the carbon cycle. These ubiquitous single-celled marine calcifying phytoplankton are re- sponsible for half of the calcium carbonate production in the modern surface ocean, and their adorning calcite plates (coccoliths), produced intracellularly, have con- tributed to sedimentary carbonate for over 200 million years. They constitute a significant control on the partitioning of carbon between the atmosphere, ocean and sedimentary reservoirs on timescales from the instantaneous to the geological. Coc- colithophores are also uniquely placed to record aspects of the carbonate chemistry of the surface ocean, because the carbon isotopic composition of the organic matter (δ13Corg) and calcite (δ13Ccal) that they produce is a function of many parameters, including ambient aqueous carbon dioxide concentration [CO2]. This thesis addresses the bidirectional interaction between coccolithophores and the carbon cycle in the geological past, by asking how cellular carbon fluxes relate to physical evidence that is preserved throughout geological time. First, I present and calibrate a novel rationale for size-normalising coccolith mass, and show that over two glacial-interglacial cycles, coccolithophores appear to calcify more under high [CO2] conditions; a result that is manifest on evolutionary timescales, and is necessarily elusive to experiments. Second, I investigate the parameters controlling δ13Ccal and δ13Corg in coccolithophores through in vivo experimentation, and devel- opment of a model of cellular isotopic fluxes. I show that so called "vital effects" in coccolithophores arise as a result of differences in calcification to photosynthesis ratios. Third, using a combination of novel and established protocols for extraction and isotopic analysis of specific organic molecules from fossils taxonomically separated by size, I show the very first size-specific geologic time series of coccolith-associated δ13Corg, and the first time-series of size-separated coccolith δ13Ccal over a glacial cycle. A novel means of inferring past carbon dioxide concentrations, based on an iterative inverse modelling approach, is presented and tested.</p

The uronic acid content of coccolith-associated polysaccharides provides an insight into coccolithogenesis and past climate

Unicellular phytoplanktonic algae (coccolithophores) are amongst the most prolific producers of calcium carbonate on the planet, with a production of ~10^26 coccoliths/year. During their lith formation, coccolithophores mainly employ coccolith-associated polysaccharides (CAPs) for the regulation of crystal nucleation and growth. These macromolecules interact with the intracellular calcifying compartment (coccolith vesicle) through the charged carboxyl groups of their uronic acid residues. Here we report the isolation of CAPs from modern day coccolithophores and their prehistoric predecessors and we demonstrate that their uronic acid content (UAC) offers a species-specific signature. We also show that there is a correlation between the UAC of CAPs and the internal saturation state of the coccolith vesicle which, for most geologically abundant species, is inextricably linked to carbon availability. These findings suggest that the UAC of CAPs reports on the adaptation of coccolithogenesis to environmental changes and is a marker for the estimation of past pCO2 concentrations

An explanation for the 18O excess in Noelaerhabdaceae coccolith calcite.

Coccoliths have dominated the sedimentary archive in the pelagic environment since the Jurassic. The biominerals produced by the coccolithophores are ideally placed to infer sea surface temperatures from their oxygen isotopic composition, as calcification in this photosynthetic algal group only occurs in the sunlit surface waters. In the present study, we dissect the isotopic mechanisms contributing to the “vital effect”, which overprints the oceanic temperatures recorded in coccolith calcite. Applying the passive diffusion model of carbon acquisition by the marine phytoplankton widely used in biogeochemical and palaeoceanographic studies, our results suggest that the oxygen isotope offsets from inorganic calcite in fast dividing species Emiliania huxleyi and Gephyrocapsa oceanica originates from the legacy of assimilated 18O-rich CO2 that induces transient isotopic disequilibrium to the internal dissolved inorganic carbon (DIC) pool. The extent to which this intracellular isotopic disequilibrium is recorded in coccolith calcite (1.5 to +3 ‰ over a 10 to 25 °C temperature range) is set by the degree of isotopic re-equilibration between CO2 and water molecules before intracellular mineralisation. We show that the extent of re-equilibration is, in turn, set by temperature through both physiological (dynamics of the utilisation of the DIC pool) and thermodynamic (completeness of the re-equilibration of the relative 18O-rich CO2 influx) processes. At the highest temperature, less ambient aqueous CO2 is present for algal growth, and the consequence of carbon limitation is exacerbation of the oxygen isotope vital effect, obliterating the temperature signal. This culture dataset further demonstrates that the vital effect is variable for a given species / morphotype, and depends on the intricate relationship between the environment and the physiology of biomineralising algae

A coastal coccolithophore maintains pH homeostasis and switches carbon sources in response to ocean acidification

WOS:000439301700001International audienceOcean acidification will potentially inhibit calcification by marine organisms; however, the response of the most prolific ocean calcifiers, coccolithophores, to this perturbation remains under characterized. Here we report novel chemical constraints on the response of the widespread coccolithophore species Ochrosphaera neapolitana (O. neapolitana) to changing-CO2 conditions. We cultured this algae under three pCO(2)-controlled seawater pH conditions (8.05, 8.22, and 8.33). Boron isotopes within the algae's extracellular calcite plates show that this species maintains a constant pH at the calcification site, regardless of CO2-induced changes in pH of the surrounding seawater. Carbon and oxygen isotopes in the algae's calcite plates and carbon isotopes in the algae's organic matter suggest that O. neapolitana utilize carbon from a single internal dissolved inorganic carbon (DIC) pool for both calcification and photosynthesis, and that a greater proportion of dissolved CO2 relative to HCO3- enters the internal DIC pool under acidified conditions. These two observations may explain how O. neapolitana continues calcifying and photosynthesizing at a constant rate under different atmospheric-pCO(2) conditions