Ocean Acidification Reduces Growth and Calcification in a Marine Dinoflagellate

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Van de Waal, Dedmer B ^a,b   John, Uwe ^a   Ziveri, Patrizia ^c,d   Reichart, Gert Jan ^e,f   Hoins, Mirja ^a,e   Sluijs, Appy ^e   Rost, Björn ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^b NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^c INSTITUT DE CIÈNCIA I TECNOLOGIA AMBIENTALS   (Spain)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e UTRECHT UNIVERSITY   (Netherlands)

^f ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CARBONATE; CARBON; CARBON DIOXIDE; ISOTOPE; OXYGEN;

ACIDIFICATION; ARTICLE; CALCIFICATION; CARBON DIOXIDE TENSION; CHEMICAL COMPOSITION; CYST; DINOFLAGELLATE; GENETIC REGULATION; GROWTH RATE; MARINE SPECIES; NONHUMAN; SEA; THORACOSPHAERA HEIMII; TRANSCRIPTOMICS;

CALCIFICATION, PHYSIOLOGIC; CARBON DIOXIDE; DINOFLAGELLIDA; HYDROGEN-ION CONCENTRATION; SEAWATER;

ANTHOZOA; DINOPHYCEAE; FORAMINIFERA; HAPTOPHYCEAE; THORACOSPHAERA HEIMII;

EID: 84878936665     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065987     Document Type: Article

References (63)

1. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, et al. (2004) The oceanic sink for anthropogenic CO2. Science 305: 367-371.
2. Le Quere C, Raupach MR, Canadell JG, Marland G, Bopp L, et al. (2009) Trends in the sources and sinks of carbon dioxide. Nature Geoscience 2: 831-836.
3. Solomon S, Qin D, Manning M, Marquis M, Averyt K, et al. (2007) Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press.
4. Wolf-Gladrow DA, Riebesell U, Burkhardt S, Bijma J, (1999) Direct effects of CO2 concentration on growth and isotopic composition of marine plankton. Tellus Series B-Chemical and Physical Meteorology 51: 461-476.
5. Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL, (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333: 418-422.
6. Moy AD, Howard WR, Bray SG, Trull TW, (2009) Reduced calcification in modern Southern Ocean planktonic foraminifera. Nature Geoscience 2: 276-280.
7. Riebesell U, Zondervan I, Rost B, Tortell PD, Zeebe RE, et al. (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407: 364-367.
8. Beaufort L, Probert I, de Garidel-Thoron T, Bendif EM, Ruiz-Pino D, et al. (2011) Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476: 80-83.
9. Ziveri P, Thoms S, Probert I, Geisen M, Langer G, (2012) A universal carbonate ion effect on stable oxygen isotope ratios in unicellular planktonic calcifying organisms. Biogeosciences 9: 1025-1032.
10. Evitt WR (1985) Sporopollen in Dinoflagellate Cysts: Their Morphology and Interpretation. Dallas, Texas, U.S.A.: American Association of Stratigraphic Palynologists Foundation.
11. Dale B, Dale AL (1992) Dinoflagellate Contributions to the Deep Sea; Honjo S, editor. Woods Hole, Massachusetts, USA: Woods Hole Oceanographic Institution.
12. Ziveri P, Broerse ATC, van Hinte JE, Westbroek P, Honjo S, (2000) The fate of coccoliths at 48 degrees N 21 degrees W, northeastern Atlantic. Deep-Sea Research Part II-Topical Studies in Oceanography 47: 1853-1875.
13. Karwath B, Janofske D, Willems H, (2000) Spatial distribution of the calcareous dinoflagellate Thoracosphaera heimii in the upper water column of the tropical and equatorial Atlantic. International Journal of Earth Sciences 88: 668-679.
14. Wendler I, Zonneveld KAF, Willems H, (2002) Production of calcareous dinoflagellate cysts in response to monsoon forcing off Somalia: a sediment trap study. Marine Micropaleontology 46: 1-11.
15. Zonneveld K, (2004) Potential use of stable oxygen isotope composition of Thoracosphaera heimii (Dinophyceae) for upper watercolumn (thermocline) temperature reconstruction. Marine Micropaleontology 50: 307-317.
16. Inouye I, Pienaar RN, (1983) Observations of the life-cycle and microanatomy of Thoracosphaera heimii (Dinophyceae) with special reference to its systematic position. South African Journal of Botany 2: 63-75.
17. Meier KJS, Young JR, Kirsch M, Feist-Burkhardt S, (2007) Evolution of different life-cycle strategies in oceanic calcareous dinoflagellates. European Journal of Phycology 42: 81-89.
18. Hildebrand-Habel T, Willems H, (2000) Distribution of calcareous dinoflagellates from the Maastrichtian to early Miocene of DSDP Site 357 (Rio Grande Rise, western South Atlantic Ocean). International Journal of Earth Sciences 88: 694-707.
19. Gussone N, Zonneveld K, Kuhnert H, (2010) Minor element and Ca isotope composition of calcareous dinoflagellate cysts of cultured Thoracosphaera heimii. Earth and Planetary Science Letters 289: 180-188.
20. Bemis BE, Spero HJ, Bijma J, Lea DW, (1998) Reevaluation of the oxygen isotopic composition of planktonic foraminifera: Experimental results and revised paleotemperature equations. Paleoceanography 13: 150-160.
21. Ziveri P, Stoll H, Probert I, Klass C, Geisen M, et al. (2003) Stable isotope 'vital effects' in coccolith calcite. Earth and Planetary Science Letters 210: 137-149.
22. Zonneveld KAF, Mackensen A, Baumann KH, (2007) Stable oxygen isotopes of Thoracosphaera heimii (Dinophyceae) in relationship to temperature; a culture experiment. Marine Micropaleontology 64: 80-90.
23. McCrea JM, (1950) On the isotopic chemistry of carbonates and a paleotemperature scale. Journal of Chemical Physics 18: 849-857.
24. Zeebe R, Wolf-Gladrow DA (2001) CO2 in Seawater: Equilibrium, Kinetics, Isotopes. Amsterdam, The Netherlands: Elsevier Science.
25. Spero HJ, Bijma J, Lea DW, Bemis BE, (1997) Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes. Nature 390: 497-500.
26. Tangen K, Brand LE, Blackwelder PL, Guillard RRL, (1982) Thoracosphaera heimii (Lohmann) Kamptner is a Dinophyte: Observations on its morphology and life-cylce. Marine Micropaleontology 7: 193-212.
27. Paasche E, (2001) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40: 503-529.
28. Pierrot DE, Lewis E, Wallace DWR (2006) MS Exel Program Developed for CO2 System Calculations. ORNL/CDIAC-105a. Oak Ridge, Tennessee, USA: Carbon Dioxide Information Analysis Centre, Oak Ridge National Laboratory, US Department of Energy.
29. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM, (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology & Oceanography 18: 897-907.
30. Dickson AG, Millero FJ, (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research Part I-Oceanographic Research Papers 34: 1733-1743.
31. Dickson AG, (1990) Standard potential of the reaction: AgCl(s) +1/2 H2(g) = Ag(s)+HCl(aq), and the standard acidity constant of the ion HSO4- in synthetic seawater from 273.15 to 318.15 K. Journal of Chemical Thermodynamics 22: 113-127.
32. Nelson ST, (2000) A simple, practical methodology for routine VSMOW/SLAP normalization of water samples analyzed by continuous flow methods. Rapid Communications in Mass Spectrometry 14: 1044-1046.
33. Mook WG, Bommerso JC, Staverma WH, (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon-dioxide. Earth and Planetary Science Letters 22: 169-176.
34. Zhang J, Quay PD, Wilbur DO, (1995) Carbon isotope fractionation during gas-water exchange and dissolution of CO2. Geochimica Et Cosmochimica Acta 59: 107-114.
35. Freeman HJ, Hayes JM, (1992) Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO2 levels. Global Biogeochem Cycles 6: 185-198.
36. Zeebe RE (2007) An expression for the overall oxygen isotope fractionation between the sum of dissolved inorganic carbon and water. Geochemistry Geophysics Geosystems 8.
37. Beck WC, Grossman EL, Morse JW, (2005) Experimental studies of oxygen isotope fractionation in the carbonic acid system at 15 degrees, 25 degrees, and 40 degrees C. Geochimica Et Cosmochimica Acta. 69: 3493-3503.
38. Quinn GP, Keough MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge, UK: Cambridge University Press.
39. Mackinder L, Bach L, Schulz K, Wheeler G, Schroeder D, et al. (2011) The molecular basis of inorganic carbon uptake mechanisms in the coccolithophore Emiliania huxleyi. European Journal of Phycology 46: 142-143.
40. Riebesell U, Schulz KG, Bellerby RGJ, Botros M, Fritsche P, et al. (2007) Enhanced biological carbon consumption in a high CO2 ocean. Nature 450: 545-U510.
41. Tortell PD, Payne CD, Li YY, Trimborn S, Rost B, et al. (2008) CO2 sensitivity of Southern Ocean phytoplankton. Geophysical Research Letters 35.
42. Bach LT, Riebesell U, Schulz KG, (2011) Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi. Limnology and Oceanography 56: 2040-2050.
43. Rokitta SD, Rost B, (2012) Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi. Limnology and Oceanography 57: 607-618.
44. Hoppe CJM, Langer G, Rost B, (2011) Emiliania huxleyi shows identical responses to elevated pCO2 in TA and DIC manipulations. Journal of Experimental Marine Biology and Ecology 406: 54-62.
45. Lohbeck KT, Riebesell U, Reusch TBH, (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geoscience 5: 346-351.
46. Collins S, Bell G, (2004) Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature 431: 566-569.
47. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology. 99-131.
48. Rost B, Zondervan I, Wolf-Gladrow D, (2008) Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: Current knowledge, contradictions and research directions. Marine Ecology Progress Series 373: 227-237.
49. Reinfelder JR (2011) Carbon Concentrating Mechanisms in Eukaryotic Marine Phytoplankton. In: Carlson CA, Giovannoni SJ, editors. Annual Review of Marine Science. 291-315.
50. Trimborn S, Lundholm N, Thoms S, Richter KU, Krock B, et al. (2008) Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: the effect of pH-induced changes in seawater carbonate chemistry. Physiologia Plantarum 133: 92-105.
51. Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R, (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425: 734-737.
52. Kranz SA, Levitan O, Richter KU, Prasil O, Berman-Frank I, et al. (2010) Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: Physiological responses. Plant Physiology 154: 334-345.
53. Sharkey TD, Berry JA (1985) Carbon isotope fractionation of algae as influenced by an inducible CO2 concentrating mechanism. In: Lucas WJ, Berry JA, editors. Inorganic carbon uptake by aquatic photosynthetic organisms. Rockville, MS, USA: American Society of Plant Physiologists.
54. Rost B, Zondervan I, Riebesell U, (2002) Light-dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi. Limnology and Oceanography 47: 120-128.
55. Taylor AR, Chrachri A, Wheeler G, Goddard H, Brownlee C (2011) A voltage-gated H+ channel underlying pH homeostasis in calcifying coccolithophores. Plos Biology 9.
56. Mackinder L, Wheeler G, Schroeder D, Riebesell U, Brownlee C, (2010) Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiology Journal 27: 585-595.
57. Taylor AR, Brownlee C, Wheeler GL, (2012) Proton channels in algae: reasons to be excited. Trends in Plant Science 17: 675-684.
58. von Dassow P, Ogata H, Probert I, Wincker P, Da Silva C, et al. (2009) Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biology 10.
59. Rokitta SD, John U, Rost B (2012) Ocean acidification affects redox-balance and ion-homeostasis in the life-cycle stages of Emiliania huxleyi. Plos One 7.
60. Beyenbach KW, Wieczorek H, (2006) The V-type H+ ATPase: molecular structure and function, physiological roles and regulation. Journal of Experimental Biology 209: 577-589.
61. Araki Y, Gonzalez EL, (1998) V- and P-type Ca2+-stimulated ATPases in a calcifying strain of Pleurochrysis sp. (Haptophyceae). Journal of Phycology 34: 79-88.
62. Kohn M, Steinke S, Baumann KH, Donner B, Meggers H, et al. (2011) Stable oxygen isotopes from the calcareous-walled dinoflagellate Thoracosphaera heimii as a proxy for changes in mixed layer temperatures off NW Africa during the last 45,000 yr. Palaeogeography Palaeoclimatology Palaeoecology 302: 311-322.
63. Zeebe RE, (1999) An explanation of the effect of seawater carbonate concentration on foraminiferal oxygen isotopes. Geochimica Et Cosmochimica Acta 63: 2001-2007.