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Coccolithophores represent a major component of the marine phytoplankton and contribute to the bulk of biogenic calcite formation on Earth. These unicellular protists produce minute calcite scales (coccoliths) within the cell, which are secreted to the cell surface. Individual coccoliths and their arrangements on the cell surface display a wide range of morphological variations. This review explores some of the recent evidence that points to similarities and differences in the mechanisms of calcification, focussing on the transport mechanisms that bring substrates to, and remove products from the site of calcification, together with new findings on factors that regulate coccolith morphology. We argue that better knowledge of these mechanisms and their variations is needed to inform more generally how different species of coccolithophore are likely to respond to changes in ocean chemistry. Coccolithophores, minute single celled phytoplankton are the major producers of biogenic carbonate on Earth. They also represent an important component of the ocean's biota and contribute significantly to global carbon fluxes. Coccolithophores produce intricate calcite scales (coccoliths) internally that they secrete onto their external surface. This review presents some recent key findings on the mechanisms underlying the production of coccoliths. It also considers the factors that regulate the rate of production as well as the variety of shapes of individual coccoliths and their arrangements at the cell surface. Understanding these processes is needed to allow better predictions of how coccolithophores may respond to changing ocean chemistry associated with climate change. Image, graphical abstract [ABSTRACT FROM AUTHOR]

Coccolithophores are important contributors to global calcium carbonate through their species-specific production of calcite coccoliths. Nannofossil coccolith calcite remains an important tool for paleoreconstructions through geochemical analysis of isotopic and trace element incorporation including Sr, which is a potential indicator of past surface ocean temperature and productivity. Scyphosphaera apsteinii (Zygodiscales) exhibits an unusually high Sr/Ca ratio and correspondingly high partitioning coefficient (D Sr = 2.5) in their two morphologically distinct types of coccoliths: flat muroliths and barrel-like lopadoliths. Whether or not this reflects mechanistic differences in calcification compared to other coccolithophores is unknown. We therefore examined the possible role of Sr in S. apsteinii calcification by growing cells in deplete (0.33 mmol/mol Sr/Ca), ambient (9 mmol/mol Sr/Ca), and higher than ambient Sr conditions (36 and 72 mmol/mol Sr/Ca). The effects on growth, quantum efficiency of photosystem II (F v /F m), coccolith morphology, and calcite D Sr were evaluated. No effect on S. apsteinii growth rate or F v /F m was observed when cells were grown in Sr/Ca between 0.33–36 mmol/mol. However, at 72 mmol/mol Sr/Ca growth rate was significantly reduced, although F v /F m was unaffected. Reducing the Sr/Ca from ambient (9 mmol/mol) did not significantly alter the frequency of malformed and aberrant muroliths and lopadoliths, but at higher than ambient Sr/Ca conditions coccolith morphology was significantly disrupted. This implies that Sr is not a critical determining factor in normal coccolith calcite morphology in this dimorphic species. Using energy dispersive spectroscopy (EDS) we observed an increase in [Sr] and decrease in D Sr of coccoliths as the Sr/Ca of the growth medium increased. Interestingly, muroliths had significantly lower Sr/Ca than lopadoliths at ambient and elevated [Sr], and lopadolith tips had lower Sr than bases in ambient conditions. In summary, the Sr fractionation behavior of S. apsteinii is distinct from other coccolithophores because of an unusually high D Sr and inter- and intra-coccolith variability in Sr/Ca. These observations could be explained by mechanistic differences in the selectivity of the Ca2+ transport pathway or in the Sr-and Ca-binding capacity of organic components, such as polysaccharides associated with coccolithogenesis. [ABSTRACT FROM AUTHOR]

It has long since been noted that minor element (Me) partitioning into biogenic carbonates is sometimes different from Me partitioning into inorganically precipitated carbonates. The prime example is the partitioning coefficient, which might be lower or even higher than the one of inorganically precipitated carbonate. Such a difference is usually termed “vital effect” and is seen as indicative of a biologically modified minor element partitioning. Over the last three decades interest in conceptual biomineralization models compatible with minor element and isotope fractionation has been steadily increasing. However, inferring features of a biomineralization mechanism from Me partitioning is complicated, because not all partitioning coefficients show vital effects in every calcium carbonate producing organism. Moreover, the partitioning coefficient is not the only aspect of Me partitioning. Other aspects include polymorph specificity and rate dependence. Patellogastropod limpets are ideally suited for analysing Me partitioning in terms of biomineralization models, because they feature both aragonitic and calcitic shell parts, so that polymorph specificity can be tested. In this study, polymorph-specific partitioning of the minor elements Mg, Li, B, Sr, and U into shells of the patellogastropod limpet Patella caerulea from within and outside a CO 2 vent site at Ischia (Italy) was investigated by means of LA-ICP-MS. The partitioning coefficients of U, B, Mg, and Sr (in aragonite) differed from the respective inorganic ones, while the partitioning coefficients of Li and Sr (in calcite) fell within the range of published values for inorganically precipitated carbonates. Polymorph specificity of Me partitioning was explicable in terms of inorganic precipitation in the case of Sr and Mg, but not Li and B. Seawater carbon chemistry did not have the effect on B partitioning that was expected on the basis of data on inorganic precipitates and foraminifera. Carbon chemistry did affect Mg (in aragonite) and Li, but only the effect on Mg was explicable in terms of calcification rate. On the one hand, these results show that Me partitioning in P. caerulea is incompatible with a direct precipitation of shell calcium carbonate from the extrapallial fluid. On the other hand, our results are compatible with precipitation from a microenvironment formed by the mantle. Such a microenvironment was proposed based on data other than Me partitioning. This is the first study which systematically employs a multi-element, multi-aspect approach to test the compatibility of Me partitioning with different conceptual biomineralization models. [ABSTRACT FROM AUTHOR]

In present day paleoclimate research one of the most pressing challenges is the reconstruction of atmospheric CO 2 concentrations. A variety of proxies for several components of the marine inorganic carbon system have been developed in this context (e.g. B isotopes, B/Ca, U/Ca) to allow reconstruction of past seawater pH, HCO 3 − and CO 3 2− and thereby facilitate estimates of past atmospheric p CO 2 . Based on culture experiments using the benthic foraminifera Ammonia sp. we describe a positive correlation between Sr/Ca and the carbonate system, namely DIC/bicarbonate ion concentration. Foraminiferal Sr/Ca ratios provide potentially additional constraints on the carbonate system proxy, because the analysis of foraminiferal carbonate Sr/Ca is straightforward and not easily contaminated. Applying our calibration to a published dataset of paleo-Sr/Ca suggests the validity of Sr/Ca as a carbonate system proxy. Furthermore, we explore how our data can be used to advance conceptual understanding of the foraminiferal biomineralization mechanism. [ABSTRACT FROM AUTHOR]

Six Emiliania huxleyi strains isolated in the Mediterranean Sea were grown under phosphorus limitation and replete (control) conditions in batch culture. We tested the hypothesis that increasing phosphorus limitation, resulting from ocean warming, will affect coccolithophores and change their contribution to the PIC:POC ratios. Four strains were isolated in the oligotrophic Algerian basin (western Mediterranean), and two strains in the extremely oligotrophic and often phosphorus depleted Levantine basin (eastern Mediterranean). Samples for particulate inorganic carbon, PIC; particulate organic carbon, POC; particulate organic phosphorus, POP; and total particulate nitrogen, TPN, were taken at equal cell densities in phosphorus limited and control culture conditions (harvesting in exponential and stationary phases respectively). Different morphological features of coccoliths were analyzed. Phosphorus limitation was inferred from: 1. a decrease in growth rate between 22% and 34% compared to phosphorus replete cultures; 2. a reduction in final cell density from ca. 2x10=sup=6=/sup=cells/ml to ca. 8x10=sup=4=/sup=cells/ml, and 3. markedly lower POP quotas of the limited cells. Differences in the phosphate uptake machinery are suggested based on the fact that three western Mediterranean strains decreased the phosphate concentration in the culture media until the detection limit in the first 3 experimental days while 4-5days were necessary for the other strains. Cellular carbon quotas increased in all strains under phosphorus limitation in comparison to their respective control cultures. The increase in POC quotas ranged between 179% and 260% and in PIC quotas between 43% and 201%. TPN quotas increased under phosphorus limitation between 31% and 86% in five out of six strains. POC:TPN increased in all strains, which suggests a change in the molecular composition of the cells when exposed to phosphorus limitation. Strain specific responses were also observed in the PIC:POC ratio, which decreased in five strains and did not change in another. Phosphorus limitation did not lead to malformations. However, morphological changes of coccoliths occurred, also in a strain specific way, namely the percentage of over-calcified coccoliths was altered by P limitation, but we observed all signs in the responses among different strains. Nevertheless, this morphological feature does not reflect the changes in calcite production (PICp nor PIC:POC). Strain specific responses were not related to the isolation location, suggesting that the isolated western and eastern strains do not represent distinct eco-genotypes featuring different phosphorus usage strategies. [ABSTRACT FROM AUTHOR]

Abstract: The coccolithophore Emiliania huxleyi (PML B92/11) was grown in batch culture under nitrogen (N) as well as phosphorus (P) limitation. Growth rate, particulate inorganic carbon (PIC), particulate organic carbon (POC), particulate organic nitrogen (PON), and particulate organic phosphorus (POP) production were determined. While PON production decreased by 96% under N-limitation and POP production decreased by 85% under P-limitation, growth rate decreased by 31% under N- and by 26% under P-limitation. POC production increased by a factor of 1.5 under N-limitation and by a factor of 3.3 under P-limitation. PIC production increased by a factor of 1.2 under N-limitation and did not change under P-limitation. It is concluded that the decrease in PON production under N-limitation and the decrease in POP production under P-limitation represent a physiological response of the cells while the increase in particulate carbon production represents a methodological artefact. The latter conclusion is based on a direct comparison of this strain's responses to nutrient limitation in different experimental setups, i.e., batch-, semi-continuous-, and continuous cultures. [Copyright &y& Elsevier]

Abstract: Calcareous foraminifera are well known for their CaCO3 shells. Yet, CaCO3 precipitation acidifies the calcifying fluid. Calcification without pH regulation would therefore rapidly create a negative feedback for CaCO3 precipitation. In unicellular organisms, like foraminifera, an effective mechanism to counteract this acidification could be the externalization of H+ from the site of calcification. In this study we show that a benthic symbiont-free foraminifer Ammonia sp. actively decreases pH within its extracellular microenvironment only while precipitating calcite. During chamber formation events the strongest pH decreases occurred in the vicinity of a newly forming chamber (range of gradient ~100μm) with a recorded minimum of 6.31 (<10μm from the shell) and a maximum duration of 7h. The acidification was actively regulated by the foraminifera and correlated with shell diameters, indicating that the amount of protons removed during calcification is directly related to the volume of calcite precipitated. The here presented findings imply that H+ expulsion as a result of calcification may be a wider strategy for maintaining pH homeostasis in unicellular calcifying organisms. [Copyright &y& Elsevier]

Abstract: Coccolithophorid algae are microscopic but prolific calcifiers in modern and ancient oceans. When the pH of seawater is modified, as may occur in the future due to ocean acidification, different species and strains of coccolithophorids have exhibited diverse calcification responses in laboratory culture. Since their biomineralization is a completely intracellular process, it is unclear why their response should be affected by extracellular seawater pH. Variations in the B/Ca in coccoliths are potential indicators of pH shifts in the intracellular coccolith vesicle where calcification occurs, because B/Ca in abiogenic calcites increases at higher pH due to the greater abundance of borate ions, the only B species incorporated into calcite. We used a SIMS ion probe to measure B/Ca of coccoliths from three different strains of Emiliania huxleyi and one strain of Coccolithus braarudii braarudii cultured under different seawater pH conditions to ascertain if the B/Ca can be used to elucidate how coccolithophorids respond to changing ocean pH. These data are interpreted with the aid of a conceptual model of cellular boron acquisition by coccolithophorids. Based on uptake in other plants, we infer that boron uptake by coccolithophorid cells is dominated by passive uptake of boric acid across the lipid bilayer. Subsequently, in the alkaline coccolith vesicle (C.V.), boron speciates according to the C.V. pH, and borate is incorporated into the coccolith. At increasing seawater pH, the relative abundance of the neutral boric acid in seawater decreases, lowering the potential B flux into the cell. Homeostasis or constant pH of the coccolith vesicle results in a decrease of the B/Ca in the coccolith with increasing seawater pH. In contrast, if coccolith vesicle pH increases with increasing seawater pH, then the B/Ca will increase as the fraction of borate in the coccolith vesicle increases. The coccolith B/Ca is also expected to depend inversely on the dissolved inorganic carbon (DIC) concentration in the coccolith vesicle. The B/Ca in cultured coccoliths is much lower than that of foraminifera or corals and limits precision in the analysis. Modest variations in DIC or pH of the coccolith vesicle can account for the observed trends in B/Ca in cultured coccoliths. The model shows that paired measurements of B/Ca and B isotopic composition of the calcite could distinguish between regulation of pH or DIC in the coccolith vesicle. [Copyright &y& Elsevier]

Abstract: The coccolithophore Calcidiscus leptoporus was grown in batch culture under nitrogen (N) as well as phosphorus (P) limitation. Growth rate, particulate inorganic carbon (PIC), particulate organic carbon (POC), particulate organic nitrogen (PON), and particulate organic phosphorus (POP) production were determined and coccolith morphology was analysed. While PON production decreased by 70% under N-limitation and POP production decreased by 65% under P-limitation, growth rate decreased by 33% under N- as well as P-limitation. POC as well as PIC production (calcification rate) increased by 27% relative to the control under P-limitation, and did not change under N-limitation. Coccolith morphology did not change in response to either P or N limitation. While these findings, supported by a literature survey, suggest that coccolith morphogenesis is not hampered by either P or N limitation, calcification rate might be. The latter conclusion is in apparent contradiction to our data. We discuss the reasons for this inference. [Copyright &y& Elsevier]

Abstract: The coccolithophore Emiliania huxleyi was grown in seawater under different Ba concentrations. The relationship of coccolith Ba/Ca ratio and seawater Ba/Ca ratio was found to be linear. The linear regression yields the apparent Ba exchange coefficient of 0.10. Our data support a recently proposed generic model (Langer G., Gussone N., Nehrke G., Riebesell U., Eisenhauer A., Kuhnert H., Rost B., Trimborn S., and Thoms S. (2006) Coccolith strontium to calcium ratios in Emiliania huxleyi: the dependence on seawater strontium and calcium concentrations. Limnol. Oceanogr. 51, 310–320.) developed for explaining apparent exchange coefficients of metabolically inert divalent trace metals, such as Sr, in E. huxleyi. This model represents the first approach combining cell physiological processes and data from inorganic precipitation experiments, which quantitatively explains coccolith apparent Sr and Ba exchange coefficients. [Copyright &y& Elsevier]

A combined culture and field study was conducted in order to (1) more firmly identify the physiological controls on hydrogen isotopic composition of C 37 alkenones produced by open-ocean coccolithophores and (2) determine the degree to which these controls are manifested in a natural water column. Nutrient-limitation experiments in culture, combined with previously published data, show that net fractionation between the growth medium and alkenones ( α K37 ) varies with cellular alkenone content and production rate, and, by extension, growth phase. It is hypothesized that the relationship of α K37 with cellular alkenone content and production rate is due to increased use of anabolic NADPH in response to high rates of lipid synthesis. Euphotic zone profiles of δD K37 , measured in suspended material from the Gulf of California and Eastern Tropical North Pacific, decreased with depth and light availability, and did not correlate in any expected way with previously-suggested controls on α K37 . It is possible that the field data are driven by behavior in light-limited cells that is not represented by the available, nutrient-limited culture data. If true, δD K37 may have utility as an indicator of production depth in settings prone to subsurface production maxima. Relationships between α K37 , cell density, and the carbon-isotopic fractionation term ε p , however, suggest that α K37 acts an indicator of growth rate, which in this setting is only partially dependent on light, consistent with our interpretation of the culture data. If this latter interpretation proves correct, δD K37 may be a powerful ecological proxy specific to these climatically-important, calcifying, temperature-encoding species. [ABSTRACT FROM AUTHOR]

Here we present the first multi-species comparison of modern and fossil coccolith trace metal data obtained from single liths. We present both trace metal analyses (Sr, Ca, Mg and Al) and distribution maps of individual Paleogene fossil coccoliths obtained by Secondary Ion Mass Spectrometry (SIMS). We use this data to determine the effects of variable coccolith preservation and diagenetic calcite overgrowths on the recorded concentrations of strontium and magnesium in coccolith calcite. The analysis of coccoliths from deep-ocean sediments spanning the Eocene/Oligocene transition demonstrates that primary coccolith calcite is resistant to the neomorphism that is common in planktonic foraminifera from similar depositional environments. Instead, where present, diagenetic calcite forms distinct overgrowths over primary coccolith calcite rather than replacing this calcite. Diagenetic overgrowths on coccoliths are easily distinguished in SIMS analyses on the basis of relatively higher Mg and lower Sr concentrations than co-occurring primary coccolith calcite. This interpretation is confirmed by the comparable SIMS analyses of modern cultured coccoliths of Coccolithus braarudii . Further, with diagenetic calcite overgrowth being the principle source of bias in coccolith-based geochemical records, we infer that lithologies with lower carbonate content, deposited below the palaeo-lysocline, are more likely to produce geochemical records dominated by primary coccolith calcite than carbonate-rich sediments where overgrowth is ubiquitous. The preservation of primary coccolith carbonate in low-carbonate lithologies thus provides a reliable geochemical archive where planktonic foraminifera are absent or have undergone neomorphism. [ABSTRACT FROM AUTHOR]

Abstract: Information on interaction of C and N at the cellular level is lacking for ecologically relevant phytoplankton species. We examined the effects of NO3 - availability on C and N fluxes in the widely distributed marine coccolithophore Emiliania huxleyi. Cells were cultured at replete (∼280μM) and ambient (∼10μM) NO3 -, the latter representing a typical surface water nitrate concentration of the North Atlantic Ocean during spring. While growth rates and C to N ratios were not altered by the NO3 - availability, organic C and N as well as inorganic C quotas were reduced under ambient NO3 -. Growth at ambient NO3 - caused a higher proportion of fixed C to be allocated to lipids relative to carbohydrates and especially to proteins. Ambient NO3 --grown cells showed lower Vmax of nitrate reductase (NR) and nitrite reductase (NiR) (ambient/replete: Vmax NR =0.64/1.09 fmol min-1 cell-1; Vmax NiR = 0.3/0.56 fmol min-1 cell-1), whereas they had higher Vmax of glutamine synthetase (GS) and glutamate synthase (GOGAT) (ambient/replete: Vmax GS =0.57/0.38 fmol min-1 cell-1; Vmax GOG =3.91/2.87 fmol min-1 cell-1). In these cells, photosynthetic O2 evolution and HCO3 - uptake rates were lower as compared to replete NO3 --grown cells (ambient/replete: Vmax O2 = 6.5/12.9 fmol min-1 cell-1; Vmax HCO3 - = 2.8/8.1 fmol min-1 cell-1). The CO2 uptake and the maximum light use efficiency of photosynthesis (α) were unaffected by the concentration of NO3 -. The affinities of NR for NO3 -, of NiR for NO2 -, of GS for Glu, and of the inorganic carbon uptake system for HCO3 - were higher under ambient NO3 - (ambient/replete: Km NR =0.074/0.099mM; Km NiR =1.69/3.14mM; Km GS =1.62/3.81mM; Km HCO3 - = 195/524μM). Our data suggest that a concerted regulation of the intracellular CO2 and NO3 - concentrations is required to maintain balanced C and N metabolic fluxes resulting in a constant C to N ratio. [Copyright &y& Elsevier]