Influence of changing carbonate chemistry on morphology and weight of coccoliths formed by Emiliania huxleyi

Biogeosciences

Volumn 9, Issue 8, 2012, Pages 3449-3463

  Bach, L T ^a   Bauke, C ^b   Meier, K J S ^b   Riebesell, U ^a   Schulz, K G ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

^b UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE; BODY SIZE; CALCIFICATION; CALCIUM CARBONATE; COCCOLITH; DISSOLUTION; GROWTH RATE; MARINE ECOSYSTEM; MORPHOLOGY; PHYTOPLANKTON; PRIMARY PRODUCTION; SEDIMENT CORE; WATER COLUMN;

EMILIANIA HUXLEYI; HAPTOPHYCEAE;

EID: 84865761128     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-9-3449-2012     Document Type: Article

References (72)

1. Bach, L. T., Riebesell, U., and Schulz, K. G.: Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi, Limnol. Oceanogr., 56, 2040-2050, 2011.
2. Batvik, H., Heimdal, B. R., Fagerbakke, K. M., and Green, J. C.: Effects of unbalanced nutrient regime on coccolith morphology and size in Emiliania huxleyi (Prymnesiophyceae), Eur. J. Phy-col., 32, 155-165, 1997. (Pubitemid 28060790)
3. Beaufort, L. and Dollfus, D.: Automatic recognition of coccolith by dynamical neural network, Mar. Micropaleont., 51, 57-73, 2004. (Pubitemid 38498112)
4. Beaufort, L., Couapel, M., Buchet, N., Claustre, H., and Goyet, C.: Calcite production by coccolithophores in the south east Pacific Ocean, Biogeosciences, 5, 1101-1117, doi:10.5194/bg-5-1101-2008, 2008.
5. Beaufort, L., Probert, I., de Garidel-Thoron, T., Bendif, E. M., Ruiz-Pino, D., Metzl, N., Goyet, C., Buchet, N., Coupel, P., Grelaud, M., Rost, B., Rickaby, R. E. M., and de Vargas, C.: Sensitivity of coccolithophores to carbonate chemistry and ocean acidification, Nature, 476, 80-83, 2011.
6. Bollmann, J. and Herrle, J. O.: Morphological variation of Emilia-nia huxleyi and sea surface salinity, Earth Planet. Sci. Lett., 255, 273-288, 2007. (Pubitemid 46323327)
7. Borman, A. H., De Jong, E. W., Huizinga, M., Kok, D. J., West-broek, P., and Bosch, L.: The role in CaCO3 crystallization of an acid Ca2+binding polysaccharide associated with coccoliths of Emiliania huxleyi, Eur. J. Biochem., 129, 179-183, 1982.
8. Bown, P. R., Lees, J. A., and Young, J. R.: Calcareous nannoplank-ton evolution and diversity through time, in: Coccolithophores-From Molecular Processes to Global Impact, edited by: Thier-stein, H. R. and Young, J. R., Springer, Heidelberg, 481-508, 2004.
9. Brand, L. E.: Genetic variability and spatial patterns of genetic differentiation in the reproductive rates of the marine coccol-ithophores Emiliania huxleyi and Gephyrocapsa oceanica, Lim-nol. Oceanogr., 27, 236-245, 1982.
10. Buitenhuis, E. T., de Baar, H. J. W., and Veldhuis, M. J. W.: Photosynthesis and calcification by Emiliania huxleyi (Prymnesio-phyceae) as a function of inorganic carbon species, J. Phycol., 35, 949-959, 1999. (Pubitemid 29530798)
11. Buitenhuis, E. T., Pangerc, T., Franklin, D. J., Le Quéré, C., and Ma-lin, G.: Growth rates of six coccolithophorid strains as a function of temperature, Limnol. Oceanogr., 53, 1181-1185, 2008. (Pubitemid 351821711)
12. De Jong, E. W., Bosch, L., and Westbroek, P.: Isolation and characterization of a Ca2+binding polysaccharide associated with coccoliths of Emiliania huxleyi (Lohmann) Kamptner, Eur. J. Biochem., 70, 611-621, 1976.
13. Dickson, A. G., Afghan, J. D., and Anderson, G. C.: Reference materials for oceanic CO2 analysis: A method for the certification of total alkalinity, Mar. Chem., 80, 185-197, 2003. (Pubitemid 36229826)
14. Dickson, A. G., Sabine, C. L., and Christian, J. R.: Guide to best practices for ocean CO2 Measurements, PICES Special Publication, Sidney, 2007.
15. Didymus, J. M., Young, J. R., and Mann, S.: Construction and morphogenesis of the chiral ultrastructure of coccoliths from the marine alga Emiliania huxleyi, Proc. R. Soc. London B, 258, 237-245, 1994.
16. Fagerbakke, K., M., Heldal, M., Norland, S., Heimdal, B. R., and Batvik, H.: Emiliania huxleyi. Chemical composition and size of coccoliths from enclosure experiments and a Norwegian fjord, Sarsia, 79, 349-355, 1994.
17. Fielding, S. R., Herrle, J. O., Bollmann, J., Worden, R. H., and Mon-tagnes, D. J. S.: Assessing the applicability of Emiliania huxleyi coccolith morphology as a sea-surface salinity proxy, Limnol. Oceanogr., 54, 1475-1480, 2009.
18. Gattuso, J. P., Gao, K., Lee, K., Rost, B. and Schulz, K. G.: Approaches and tools to manipulate the carbonate chemistry, in: Guide for best practices for ocean acidification research and data reporting, edited by: Riebesell, U., Fabry, V., Hansson, L., and Gattuso, J. P., Publications Office of the European Union, 41-52, 2010.
19. Green, J. C., Heimdal, B. R., Paasche, E., and Moate, R.: Changes in calcification and the dimensions of coccoliths of Emiliania huxleyi (Haptophyta) grown at reduced salinities, Phycologia, 37, 121-131, 1998. (Pubitemid 29424815)
20. Guillard, R. R. and Ryther, J. H.: Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran, Can. J. Microbiol., 8, 229-239, 1962.
21. Hagino, K., Bendif, E. M., Young, J. R., Kogame, K., Probert, I., Takano, Y., Horiguchi, T. de Vargas, C., and Okada, H.: New evidence for morphological and genetic variation in the cosmopolitan coccolithophore Emiliania huxleyi (Prymnesiophyceae) from the COX1b-ATP4 genes, J. Phycol., 47, 1164-1176, 2011.
22. Halloran, P. R., Hall, I. R., Colmenero-Hidalgo, E., and Rick-aby, R. E. M.: Evidence for a multi-species coccolith volume change over the past two centuries: understanding a potential ocean acidification response, Biogeosciences, 5, 1651-1655, doi:10.5194/bg-5-1651-2008, 2008.
23. Hansen, H. P. and Koroleff, F.: Determination of nutrients, in: Methods of seawater analysis, edited by: Grasshoff, K., Kremling, K., and Ehrhardt, M., Wiley-VCH, 159-228, 1999.
24. Henriksen, K. and Stipp, S. L., S.: Controlling Biomineralization: The Effect of Solution Composition on Coccolith Polysaccharide Functionality, Cryst. Growth Des., 9, 2088-2097, 2009.
25. Henriksen, K., Stipp, S. L. S., Young, J. R., and Marsh, M. E.: Biologic control on calcite crystallization: AFM investigation of coccolith polysaccharide function, Am. Mineralogist, 89, 1709-1716, 2004. (Pubitemid 40032636)
26. Holligan, P. M., Fernandez, E., Aiken, J., Balch, W. M., Boyd, P., Burkill, P. H., Finch, M., Groom, S. B., Malin, G., Muller, K., Purdie, D. A., Robinson, C., Trees, C. C., Turner, S. M., and van der Wal, P.: A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic, Global Biogeochem. Cy., 7, 879-900, 1993.
27. Honjo, S.: Coccoliths: Production, transportation and sedimentation, Mar. Micropaleontol., 1, 65-79, 1976.
28. Iglesias-Rodriguez, M. D., Schofield, O. M., Batley, J., Medlin, L. K., and Hayes, P. K.: Intraspecific genetic diversity in the marine coccolithohore Emiliania huxleyi (Prymnesiophyceae): The use of microsatellite analysis in marine phytoplankton population studies, J. Phycol., 42, 526-536, 2006. (Pubitemid 43807262)
29. Iglesias-Rodriguez, M. D., Halloran, P. R., Rickaby, R. E. M., Hall, I. R., Colmenero-Hidalgo, E., Gittins, J. R., Green, D. R. H., Tyrrell, T., Gibbs, S. J., von Dassow, P., Rehm, E., Armbrust, E. V., and Boessenkool, K. P.: Phytoplankton calcification in a high-CO2 world, Science, 320, 336-340, doi:10.1126/science.1154122, 2008. (Pubitemid 351555651)
30. Kaffes, A., Thoms, S., Trimborn, S., Rost, B., Langer, G., Richter, K.-U., Köhler, A., Norici, A., and Giordano, M.: Carbon and nitrogen fluxes in the marine coccolithophore Emiliania huxleyi grown under different nitrate concentrations, J. Exp. Mar. Biol. Ecol., 393, 1-8, 2010.
31. Kester, D., Duedall, I. W., Connors, D. N., and Pytkowicz, R. M.: Preparation of artificial seawater, Limnol. Oceanogr., 1, 176-179, 1967.
32. Langer, G. and Bode, M.: CO2 mediation of adverse effects of sea-water acidification in Calcidiscus leptoporus, Geochem. Geophy. Geosy., 12, Q05001, doi:10.1029/2010GC003393, 2011.
33. Langer, G., Geisen, M., Baumann, K.-H., Kläs, J., Riebesell, U., Thoms, S. and Young, J. R.: Species-specific responses of calcifying algae to changing seawater carbonate chemistry, Geochem. Geophy. Geosy., 7, Q09006, doi:10.1029/2005GC001227, 2006.
34. Langer, G., Gussone, N., Nehrke, G., Riebesell, U., Eisenhauer, A., and Thoms, S.: Calcium isotope fractionation during coc-colith formation in Emiliania huxleyi: Independence of growth and calcification rate, Geochem. Geophys. Geosys., 8, Q05007, doi:10.1029/2006GC001422, 2007.
35. Langer, G., Nehrke, G., Probert, I., Ly, J., and Ziveri, P.: Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry, Biogeosciences, 6, 2637-2646, doi:10.5194/bg-6-2637-2009, 2009.
36. Langer, G., De Nooijer, L. J., and Oetjen, K.: On the role of the cy-toskeleton in coccolith morphogenesis: the effect of cytoskeleton inhibitors, J. Phycol., 46, 1252-1256, 2010.
37. Langer, G., Probert, I., Nehrke, G., and Ziveri, P.: The morphological response of Emiliania huxleyi to seawater carbonate chemistry changes: an inter-strain comparison, J. Nannoplankton Res., 32, 29-34, 2011.
38. LaRoche, J., Rost, B., and Engel, A.: Bioassay, batch culture and chemostat experimentation, in: Guide for best practices for ocean acidification research and data reporting, edited by: Riebesell, U., Fabry, V., Hansson, L., and Gattuso, J.-P., Publications Office of the European Union, 81-94, 2010.
39. 2 System Calculations ORNL/CDIAC-105, Carbon Dioxide Information Analysis Centre, Oak Ridge National Laboratory, US Department of Energy, 1998. Molecular mechanisms underlying calcification in coccolithophores, Geomicrobiol. J., 27, 585-595, 2010.
40. Mackinder, L. C. M., Wheeler, G., Schroeder, D., von Das-sow, P., Riebesell, U., and Brownlee, C.: Expression of biomineralization-related ion transport genes in Emiliania hux-leyi, Environ. Microbiol., 13, 3250-3265, 2011.
41. Marsh, M. E.: Polyanion-mediated mineralization-assembly and reorganization of acidic polysaccharides in the Golgi system of a coccolithophorid alga during mineral deposition, Protoplasma, 177, 108-122, 1994. (Pubitemid 2058457)
42. Moore, T. S., Dowell, M. D., and Franz, B. A.: Detection of coccol-ithophore blooms in ocean color satellite imagery: A generalized approach for use with multiple sensors, Remote Sens. Environ., 117, 249-263, 2012.
43. Müller, M. N., Schulz, K. G., and Riebesell, U.: Effects of long-term high CO2 exposure on two species of coccolithophores, Biogeo-sciences, 7, 1109-1116, doi:10.5194/bg-7-1109-2010, 2010.
44. Paasche, E.: Roles of nitrogen and phosphorus in coccolith formation in Emiliania huxleyi (Prymnesiophyceae), Eur. J. Phycol., 33, 33-42, 1998.
45. Paasche, E.: A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coc-colith formation, and calcification-photosynthesis interactions., Phycologia, 40, 503-529, 2002.
46. Ploug, H., Iversen, M. H., Koski, M., and Buitenhuis, E. T.: Production, oxygen respiration rates, and sinking velocity of cope-pod fecal pellets: Direct measurements of ballasting by opal and calcite, Limnol. Oceanogr., 53, 469-476, 2008. (Pubitemid 351705400)
47. Raffi, I., Backman, J., Fornaciari, E., Pälike, H., Rio, D., Lourens, L., and Hilgen, F.: A review of calcareous nannofossil astro-biochronology encompassing the past 25 million years, Quat. Sci. Rev., 25, 3113-3137, 2006. (Pubitemid 46209384)
48. Raven, J. A., Caldeira, K., Elderfield, H., Hoegh-Guldberg, O., Liss, P., Riebesell, U., Shepherd, J., Turley, C., and Watson, A.: Ocean acidification due to increasing atmospheric carbon dioxide, 60, Policy Document 12/05, The Royal Society, London, 2005.
49. Riebesell, U. and Tortell, P. D.: Effects of ocean acidification on pelagic organisms and ecosystems, in: ocean acidification, edited by: Gattuso, J.-P. and Hansson, L., Oxford University Press, Oxford, 99-121, 2011.
50. Riebesell, U., Zondervan, I., Rost, B., Tortell, P. D., Zeebe, R., and Morel, M. F. M.: Reduced calcification of marine plankton in response to increased atmospheric CO2, Nature, 407, 364-367, 2000.
51. Roy, R. N., Roy, L. N., Vogel, K. M., Porter-Moore, C., Pearson, T., Good, C. E., Millero, F. J., and Campbell, D. C.: Thermodynamics of the dissociation of boric acid in seawater at S 5 35 from 0 degrees C to 55 degrees C, Mar. Chem., 44, 243-248, 1993. (Pubitemid 24430331)
52. Sarmiento, J. L. and Gruber, N. (Eds.): Ocean biogeochemical dynamics, Cambridge University Press, Cambridge, United States of America, 2006.
53. Schiebel, R., Brupbacher, U., Schmidko, S., Nausch, G., Waniek, J. J., and Thierstein, H.-R.: Spring coccolithophore production and dispersion in the temperate eastern North Atlantic Ocean, J. Geophys. Res., 116, C08030, doi:10.1029/2010JC006841, 2011.
54. Schulz, K. G., Riebesell, U., Bellerby, R. G. J., Biswas, H., Mey-erhöfer, M., Müller, M. N., Egge, J. K., Nejstgaard, J. C., Neill, C., Wohlers, J., and Zöllner, E.: Build-up and decline of organic matter during PeECE III, Biogeosciences, 5, 707-718, doi:10.5194/bg-5-707-2008, 2008. (Pubitemid 351667789)
55. Sikes, C. S., Roer, R. D., and Wilbur, K. M.: Photosynthesis and coccolith formation: inorganic carbon sources and net inorganic reaction of deposition, Limnol. Oceanogr., 25, 248-261, 1980.
56. Stoll, M. H. C., Bakker, K., Nobbe, G. H., and Haese, R. R.: Continuous-flow analysis of dissolved inorganic carbon content in seawater, Anal. Chem., 73, 4111-4116, 2001. (Pubitemid 32830850)
57. Suffrian K., Schulz, K. G., Gutowska, M., Riebesell, U., and Ble-ich, M.: Cellular pH measurements in Emiliania huxleyi reveal pronounced membrane proton permeability, New Phytol., 190, 595-608, 2011.
58. Thierstein, H. R., Geitzenauer, K., R., Molfino, B., and Shackleton, N. J.: Global synchroneity of late quaternary coccolith datum levels: validation by oxygen isotopes, Geology, 5, 400-404, 1977.
59. Triantaphyllou, M., Dimiza, M., Krasakopoulou, E., Malinverno, E., Lianou, V., and Souvermezoglou, E.: Seasonal variation in Emiliania huxleyi coccolith morphology and calcification in the Aegean Sea (Eastern Mediterranean), Geobios, 43, 99-110, 2010.
60. Tyrell, T. and Merico, A.: Emiliania huxleyi: bloom observations and the conditions that induce them, in: Coccolithophores from molecular processes to global impact, edited by: Thierstein, H.-R. and Young, J. R., Springer, Heidelberg, 2004.
61. Tyrrell, T. and Young, J. R.: Coccolithophores, in: Encyclopedia of Ocean Sciences, edited by: Steele, J. H., Turekian, K. K., and Thorpe, S. A., Academic Press, San Diego, 3568-3576, 2009.
62. van der Wal, P., De Jong, E. W., Westbroek, P., De Bruijn, W. C., and Mulder-Stapel, A. A.: Ultrastructural polysaccharide localization in calcifying and naked cells of the coccolithophorid Emiliania huxleyi, Protoplasma, 118, 157-168, 1983.
63. Watabe, N. and Wilbur, K. M.: Effects of temperature on growth, calcification and coccolith form in Coccolithus huxleyi (Coccol-ithineae), Limnol. Oceanogr., 11, 567-575, 1966.
64. Westbroek, P., De Jong, E. W., Van Der Wal, P., Borman, A. H., De Vrind, J. P. M., Kok, D., De Bruijn, W. C., and Parker, S. B.: Mechanism of calcification in the marine alga Emiliania huxleyi, Philos. Trans. R. Soc. Lond. B, 304, 435-444, 1984.
65. Westbroek, P., Young, J. R., and Linschooten, K.: Coccolith production (biomineralisation) in the marine alga Emiliania huxleyi, J. Protozool., 36, 368-373, 1989.
66. Young, J. R.: Variation in Emiliania huxleyi coccolith morphology in samples from the Norwegian EHUX mesocosm experiment, 1992, Sarsia, 79, 417-425, 1994.
67. Young, J. R. and Westbroek, P.: Genotypic variation in the coccol-ithophorid species Emiliania huxleyi, Mar. Micropaleontol., 18, 5-23, 1991.
68. Young, J. and Ziveri, P.: Calculation of coccolith volume and its use in calibration of carbonate flux estimates, Deep Sea Res., 47, 1679-1700, 2000. (Pubitemid 30427664)
69. Young, J. R., Didymus, J. M., Bown, P. R., Prins, B., and Mann, S.: Crystal assembly and evolution in heterococcoliths, Nature, 356, 516-518, 1992.
70. Young, J. R., Davis, S. A., Bown, P. R., and Mann, S.: Coccolith ultrastructure and biomineralisation, J. Struct. Biol., 126, 195-215, 1999. (Pubitemid 29402568)
71. Young, J. R., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I., and Østergaard, J. B.: A guide to extant calcareous nannoplankton taxonomy, J. Nannoplankton Res., 1, 1-125, 2003.
72. Young, J. R., Andruleit, H., and Probert, I.: Coccolith function and morphogenesis: insights from appendage-bearing coccol-ithophores of the family Syracosphaeraceae (Haptophyta), J. Phycol., 45, 213-26, 2009.