The origin of carbon isotope vital effects in coccolith calcite

Nature Communications

Volumn 8, Issue , 2017, Pages

  McClelland, H L O ^a,b   Bruggeman, J ^c   Hermoso, M ^d   Rickaby, R E M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b WASHINGTON UNIVERSITY   (United States)

^c PLYMOUTH MARINE LABORATORY   (United Kingdom)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CARBONATE; CARBON;

CALCIFICATION; CARBON FIXATION; CARBON ISOTOPE; COCCOLITH; FORAMINIFERA; ISOTOPIC COMPOSITION; PALEOCLIMATE; PALEOENVIRONMENT; PROXY CLIMATE RECORD; SHELL; TRIASSIC; ZOOPLANKTON;

ARTICLE; CARBON FIXATION; CARBON UTILIZATION; COCCOLITH; HAPTOPHYTA; THEORETICAL MODEL;

ALGAE; FORAMINIFERA; HAPTOPHYCEAE;

EID: 85014670435     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14511     Document Type: Article

References (81)

1. Hermoso, M. Isotopic record of Pleistocene glacial/interglacial cycles in pelagic carbonates: revisiting historical data from the Caribbean Sea. Quat. Sci. Rev. 137, 69-78 (2016).
2. Bolton, C. T., Stoll, H. M. Late Miocene threshold response of marine algae to carbon dioxide limitation. Nature 500, 558-562 (2013).
3. Bolton, C. T., et al. Decrease in coccolithophore calcification and CO2 since the middle Miocene. Nat. Commun. 7, 10284 (2016).
4. Ziveri, P., et al. Stable isotope 'vital effects' in coccolith calcite. Earth Planet. Sci. Lett. 210, 137-149 (2003).
5. Dudley, W., Blackwelder, P., Brand, L., Duplessy, J. Stable isotopic composition of coccoliths. Mar. Micropaleontol. 10, 1-8 (1986).
6. Hermoso, M. Coccolith-derived isotopic proxies in palaeoceanography: where geologists need biologists. Cryptogam. Algol. 35, 323-351 (2014).
7. Rickaby, R. E. M., Henderiks, J., Young, J. N. Perturbing phytoplankton: response and isotopic fractionation with changing carbonate chemistry in two coccolithophore species. Clim. Past 6, 771-785 (2010).
8. Rost, B., Zondervan, I., Riebesell, U. Light-dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi. Limnol. Oceanogr. 47, 120-128 (2002).
9. Hermoso, M., et al. Vanishing coccolith vital effects with alleviated carbon limitation. Biogeosciences 13, 301-312 (2016).
10. Fink, C., Baumann, K. H., Groeneveld, J., Steinke, S. Strontium/Calcium ratio, carbon and oxygen stable isotopes in coccolith carbonate from different grainsize fractions in South Atlantic surface sediments. Geobios 43, 151-164 (2010).
11. Henderiks, J. Coccolithophore size rules-Reconstructing ancient cell geometry and cellular calcite quota from fossil coccoliths. Mar. Micropaleontol. 67, 143-154 (2008).
12. Descolas-Gros, C., Fontungne, M. Stable carbon isotope fractionation by marine phytoplankton during photosynthesis. Plant Cell Environ. 13, 207-218 (1990).
13. Guy, R. D., Fogel, M. L., Berry, J. A. Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol. 101, 37-47 (1993).
14. Tcherkez, G. G. B., Farquhar, G. D., Andrews, T. J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl Acad. Sci. USA 103, 7246-7251 (2006).
15. Laws, E., et al. Controls on the molecular distribution and carbon isotopic composition of alkenones in certain haptophyte algae. Geochem. Geophys. Geosyst. 2, 2000GC000057 (2001).
16. Farquhar, G., O'leary, M., Berry, J. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust. J. Plant Physiol. 9, 121-137 (1982).
17. Farquhar, G. On the nature of carbon isotope discrimination in C4 species. Aust. J. Plant Physiol. 10, 205-226 (1983).
18. Sharkey, T. D., Berry, J. A. in Inorganic carbon uptake by aquatic photosynthetic organisms. (eds Lucas, W. J., Berry, J. A. ) 389-401 (American Society of Plant Physiologists, 1985).
19. Rau, G. H., Riebesell, U., Wolf-Gladrow, D. A model of photosynthetic 13C fractionation by marine phytoplankton based on diffusive molecular CO2 uptake. Mar. Ecol. Prog. Ser. 133, 275-285 (1996).
20. Francois, R., et al. Changes in the d13C of surface water particulate organic matter across the Subtropical Convergence in the SW Indian Ocean. Global Biogeochem. Cycles 7, 627-644 (1993).
21. Laws, E. A., Popp, B. N., Bidigare, R. R., Kennicutt, M. C., Macko, S. A. Dependence of phytoplankton carbon isotopic composition on growth rate and[CO2laq: Theoretical considerations and experimental results. Geochim. Cosmochim. Acta 59, 1131-1138 (1995).
22. Rau, G. H., Riebesell, U., Wolf-gladrow, D. A. CO2aq-dependent photosynthetic 13C fractionation in the ocean: a model versus measurements. Global Biogeochem. Cycles 11, 267-278 (1997).
23. Popp, B. N., et al. Effect of phytoplankton cell geometry on carbon isotopic fractionation. Geochim. Cosmochim. Acta 62, 69-77 (1998).
24. Keller, K., Morel, F. M. Model of carbon isotopic fractionation and active carbon uptake in phytoplankton. Mar. Ecol. Progr. Ser. 182, 295-298 (1999).
25. Cassar, N., Laws, E., Popp, B. N. Carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum under nutrient-and light-limited growth conditions. Geochim. Cosmochim. Acta 70, 5323-5335 (2006).
26. Schulz, K., et al. The effect of iron availability on the regulation of inorganic carbon acquisition in the coccolithophore Emiliania huxleyi and the significance of cellular compartmentation for stable carbon isotope fractionation. Geochim. Cosmochim. Acta 71, 5301-5312 (2007).
27. Hollander, D. J., McKenzie, J. A. CO2 control on carbon-isotope fractionation during aqueous photosynthesis: a paleo-pCO2 barometer. Geology 19, 929-932 (1991).
28. Pagani, M. The alkenone-CO2 proxy and ancient atmospheric carbon dioxide. Philos. Transact. A Math. Phys. Eng. Sci. 360, 609-632 (2002).
29. Pagani, M., Zachos, J., Freeman, K., Tipple, B., Bohaty, S. Marked decline in atmospheric carbon dioxide concentrations during the Paleogene. Science 309, 600-603 (2005).
30. Seki, O., et al. Alkenone and boron-based Pliocene pCO2 records. Earth Planet. Sci. Lett. 292, 201-211 (2010).
31. Pagani, M., Huber, M., Liu, Z., Bohaty, S. The role of carbon dioxide during the onset of Antarctic glaciation. Science 334, 1261-1265 (2011).
32. Laws, E. A., Bidigare, R. R., Popp, B. N. Effect of growth rate and CO2 concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum. Limnol. Oceanogr. 42, 1552-1560 (1997).
33. Anning, T., Nimer, N., Merrett, M. J., Brownlee, C. Costs and benefits of calcification in coccolithophorids. J. Mar. Syst. 9, 45-56 (1996).
34. Badger, M., Andrews, T. The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can. J. Bot. 1071, 1052-1071 (1998).
35. Falkowski, P. G., Raven, J. A. Aquatic Photosynthesis (Blackwell Science: Malden, MA, 1997).
36. Riebesell, U., Wolf-Gladrow, D. A., Smetacek, V. Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361, 249-251 (1993).
37. Rost, B., et al. Carbon acquisition of bloom-forming marine phytoplankton. Limnol. Oceanogr. 48, 55-67 (2003).
38. Kottmeier, D. M., Rokitta, S. D., Tortell, P. D., Rost, B. Strong shift from HCO3 (-) to CO 2 uptake in Emiliania huxleyi with acidification: new approach unravels acclimation versus short-term pH effects. Photosynth. Res. 121, 265-275 (2014).
39. Boller, A. J., Thomas, P. J., Cavanaugh, C. M., Scott, K. M. Low stable carbon isotope fractionation by coccolithophore RubisCO. Geochim. Cosmochim. Acta 75, 7200-7207 (2011).
40. Mackinder, L., et al. Expression of biomineralization-related ion transport genes in Emiliania huxleyi. Environ. Microbiol. 13, 3250-3265 (2011).
41. Richier, S., Fiorini, S., Kerros, M.-E., von Dassow, P., Gattuso, J.-P. Response of the calcifying coccolithophore Emiliania huxleyi to low pH/high pCO2: from physiology to molecular level. Mar. Biol. 158, 551-560 (2011).
42. Bach, L. T., et al. Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytol. 199, 121-134 (2013).
43. Aalkjaer, C., Boedtkjer, E., Choi, I., Lee, S. Cation-coupled bicarbonate transporters. Compr. Physiol. 4, 1605-1637 (2014).
44. Zeebe, R., Wolf-Gladrow, D. CO2 in Seawater: Equilibrium, Kinetics, Isotopes (Elsevier, 2001).
45. Uchikawa, J., Zeebe, R. The effect of carbonic anhydrase on the kinetics and equilibrium of the oxygen isotope exchange in the CO2-H2O system: implications for d 18 O vital effects. Geochim. Cosmochim. Acta 95, 15-34 (2012).
46. Hopkinson, B. M., Dupont, C. L., Allen, A. E., Morel, F. M. M. Efficiency of the CO2-concentrating mechanism of diatoms. Proc. Natl Acad. Sci. USA 108, 3830-3837 (2011).
47. Holtz, L.-M., Wolf-Gladrow, D., Thoms, S. Numerical cell model investigating cellular carbon fluxes in Emiliania huxleyi. J. Theor. Biol. 364, 305-315 (2014).
48. Holtz, L.-M., Wolf-Gladrow, D., Thoms, S. Simulating the effects of light intensity and carbonate system composition on particulate organic and inorganic carbon production in Emiliania huxleyi. J. Theor. Biol. 372, 192-204 (2015).
49. Nimer, N. A., IglesiasRodriguez, M. D., Merrett, M. J. Bicarbonate utilization by marine phytoplankton species. J. Phycol. 33, 625-631 (1997).
50. Herfort, L., Thake, B., Roberts, J. Acquisition and use of bicarbonate by Emiliania huxleyi. New Phytol. 156, 427-436 (2002).
51. von Dassow, P., et al. Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biol. 10, R114 (2009).
52. Richier, S., et al. Light-dependent transcriptional regulation of genes of biogeochemical interest in the diploid and haploid life cycle stages of Emiliania huxleyi. Appl. Environ. Microbiol. 75, 3366-3369 (2009).
53. Boller, A., Thomas, P., Cavanaugh, C., Scott, K. Isotopic discrimination and kinetic parameters of RubisCO from the marine bloom-forming diatom, Skeletonema costatum. Geobiology 13, 33-43 (2015).
54. Mucci, A. The solubility of calcite and aragonite in sea water at various salinities, temperatures, and one atmospheric total pressure. Am. J. Sci. 283, 780-799 (1983).
55. Kirst, G. Salinity tolerance of eukaryotic marine algae. Annu. Rev. Plant Physiol. Plant Mol. Bioi. 40, 21-53 (1989).
56. Langer, G., et al. Calcium isotope fractionation during coccolith formation in Emiliania huxleyi: independence of growth and calcification rate. Geochem. Geophys. Geosyst. 8, Q05007 (2007).
57. Langer, G., et al. Coccolith strontium to calcium ratios in Emiliania huxleyi: The dependence on seawater strontium and calcium concentrations. Limnol. Oceanogr. 51, 310-320 (2006).
58. Gussone, N., et al. Cellular calcium pathways and isotope fractionation in Emiliania huxleyi. Geology 34, 625-628 (2006).
59. Hopkinson, B. M. A chloroplast pump model for the CO2 concentrating mechanism in the diatom Phaeodactylum tricornutum. Photosynth. Res. 121, 223-233 (2014).
60. Zeebe, R. Kinetic fractionation of carbon and oxygen isotopes during hydration of carbon dioxide. Geochim. Cosmochim. Acta 139, 540-552 (2014).
61. Guo, W. Carbonate clumped isotope thermometry: application to carbonaecous chondrites and effects of kinetic isotope fractionation. Ph. D. thesis (Caltech, 2009).
62. Watkins, J. M., Hunt, J. D., Ryerson, F. J., DePaolo, D. J. The influence of temperature, pH, and growth rate on the d18O composition of inorganically precipitated calcite. Earth Planet. Sci. Lett. 404, 332-343 (2014).
63. Watkins, J. M., Nielsen, L. C., Ryerson, F. J., DePaolo, D. J. The influence of kinetics on the oxygen isotope composition of calcium carbonate. Earth Planet. Sci. Lett. 375, 349-360 (2013).
64. Lee, R. B. Y., Mavridou, D. A. I., Papadakos, G., McClelland, H. L. O., Rickaby, R. E. M. The uronic acid content of coccolith-associated polysaccharides provides insight into coccolithogenesis and past climate. Nat. Commun. 7, 13144 (2016).
65. McClelland, H. L. O., et al. Calcification response of a key phytoplankton family to millennial-scale environmental change. Sci. Rep. 6, 34263 (2016).
66. Stoll, H. M., Schrag, D. P. Coccolith Sr/Ca as a new indicator of coccolithophorid calcification and growth rate. Geochem. Geophys. Geosyst. Global Biogeochem. Cycles 1, 1006 (2000).
67. Rickaby, R. E. M., Schrag, D. P., Zondervan, I., Riebesell, U. Growth rate dependence of Sr incorporation during calcification of Emiliania huxleyi. Global Biogeochem. Cycles, 16, 1-8 (2002).
68. Berges, J. A., Franklin, D. J., Harrison, P. J. Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J. Phycol. 37, 1138-1145 (2001).
69. Keller, M., Selvin, R., Claus, W., Guillard, R. R. L. Media for the culture of oceanic ultraphytoplankton. J. Phycol. 23, 633-638 (1987).
70. Müller, M., Antia, A., LaRoche, J. Influence of cell cycle phase on calcification in the coccolithophore Emiliania huxleyi. Limnol. Oceanogr. 53, 506-512 (2008).
71. Johnson, S. G. The NLopt nonlinear-optimization package (2014).
72. Gablonsky, J., Kelley, C. A locally-biased form of the DIRECT algorithm. J. Global Optim. 21, 27-37 (2001).
73. Storn, R., Price, K. Differential evolution-a simple and efficient heuristic for global optimization over continuous spaces. J. Global Optim. 11, 341-359 (1997).
74. Nelder, J., Mead, R., Nelder, B. J. A., Mead, R. A simplex method for function minimization. Comput. J. 7, 308-313 (1964).
75. Riebesell, U., Revill, A. T., Holdsworth, D. G., Volkman, J. K. The effects of varying CO2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi. Geochim. Cosmochim. Acta 64, 4179-4192 (2000).
76. Sültemeyer, D., Rinast, K.-A. The CO2 permeability of the plasma membrane of Chlamydomonas reinhardtii: mass-spectrometric 18O-exchange measurements from 13C18O2 in suspensions of carbonic anhydrase-loaded plasma-membrane vesicles. Planta 49, 358-368 (1996).
77. Reinfelder, J. R. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Ann. Rev. Mar. Sci. 3, 291-315 (2011).
78. DOE. Handbook of methods for the analysis of the various parameters of the carbon dioxide system in sea water. Version 2 (eds Dickson, A. G, Goyet, C. ) (ORNL/CDIAC-74, 1994).
79. Lueker, T. J., Dickson, A. G., Keeling, C. D. Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Mar. Chem. 70, 105-119 (2000).
80. Bendif, E. M., Young, J. On the ultrastructure of Gephyrocapsa oceanica (haptophyta) life stages. Cryptogam. Algol. 35, 379-388 (2014).
81. Taylor, A. R., Russell, M. A., Harper, G. M., Collins, T. F. T., Brownlee, C. Dynamics of formation and secretion of heterococcoliths by Coccolithus pelagicus ssp. braarudii. Eur. J. Phycol. 42, 125-136 (2007).