The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms

Journal of Experimental Marine Biology and Ecology

Volumn 376, Issue 1, 2009, Pages 26-36

  Trimborn, Scarlett ^a   Wolf Gladrow, Dieter ^a   Richter, Klaus Uwe ^a   Rost, Björn ^a  

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

Author keywords

13C fractionation; C4 photosynthesis; CA; CCM; PEPC; RubisCO

Indexed keywords

ACCLIMATION; CARBON DIOXIDE; CONCENTRATION (COMPOSITION); DIATOM; ENZYME ACTIVITY; MASS SPECTROMETRY; PHOTOSYNTHESIS; SATURATION;

BACILLARIOPHYTA; EUCAMPIA ZODIACUS; NITZSCHIA ALBA; SKELETONEMA COSTATUM; THALASSIONEMA NITZSCHIOIDES; THALASSIOSIRA PSEUDONANA;

EID: 67649863539     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2009.05.017     Document Type: Article

References (87)

1. Armbrust E.V., Berges J.A., Bowler C., Green B.R., Martinez D., Putnam N.H., Zhou S., Allen A.E., Apt K.E., Bechner M., Brzezinski M.A., Chaal B.K., Chiovetti A., Davids A.K., Demarest M.S., Detter J.D., Glavina T., Goodstein D., Hadi M.Z., Hellsten U., Hildebrand M., Jenkins B.D., Jurka J., Kapitonov V.V., Kröger N., Lau W.W.Y., Lane T.D., Larimer F.W., Lippmeier J.C., Lucas S., Medina M., Montsant A., Obornik M., Parker M.S., Palenik B., Pazour G.J., Richardson P.M., Rynearson T.A., Saito M.A., Schwartz D.C., Thamatrakoln K., Valentin K., Vardi A., Wilkerson F.P., and Rokhsar D.S. The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science 306 (2004) 79-86
2. Asmus R. Field measurements on seasonal variation of the activity of primary producers on a sandy tidal flat in the northern Wadden Sea. Neth. J. Sea Res. 16 (1982) 389-402
3. 2 concentrating mechanisms. Photosynth. Res. 77 (2003) 83-94
4. Badger M.R., and Price G.D. Carbonic anhydrase activity associated with the cyanobacterium Synechococcus PCC7942. Plant Physiol. 89 (1989) 51-60
5. Badger M.R., and Price G.D. The role of carbonic anhydrase in photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45 (1994) 369-392
6. - fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol. Plant. 90 (1994) 529-536
7. 2-concentrating mechanisms in algae. Can. J. Bot. 76 (1998) 1052-1071
8. Brewer P.G., Bradshow A.L., and Williams R.T. Measurement of total carbon dioxide and alkalinity in the North Atlantic Ocean in 1981. In: Trabalka J.R., and Reichle D.E. (Eds). The Changing Carbon Cycle - a Global Analysis (1986), Springer, New York 358-381
9. Buesseler K.O. The decoupling of production and particulate export in the surface ocean. Glob. Biogeochem. Cycles 12 (1998) 297-310
10. 2 availability affects elemental composition (C:N:P) of the marine diatom Skeletonema costatum. Mar. Ecol. Prog. Ser. 155 (1997) 67-76
11. 2 availability. Mar. Ecol. Prog. Ser. 184 (1999) 31-41
12. 2 concentrations. Limnol. Oceanogr. 46 (2001) 1378-1391
13. Burns B.D., and Beardall J. Utilization of inorganic carbon acquisition by marine microalgae. J. Exp. Mar. Biol. Ecol. 107 (1987) 75-86
14. Cassar N., and Laws E.A. Potential contribution of ß-carboxylases to photosynthetic carbon isotope fractionation in a marine diatom. Phycologia 46 (2007) 307-314
15. Colman B., and Rotatore C. Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant Cell Environ. 18 (1995) 919-924
16. Colman B., Huertas I.E., Bhatti S., and Dason J.S. The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct. Plant Biol. 29 (2002) 261-270
17. Dason J.S., Huertas I.E., and Colman B. Source of inorganic carbon for photosynthesis in two marine dinoflagellates. J. Phycol. 40 (2004) 285-292
18. Descolas-Gros C., and Oriol L. Variations in carboxylase activity in marine phytoplankton cultures. ß-carboxylation in carbon flux studies. Mar. Ecol. Prog. Ser. 85 (1992) 163-169
19. Dickson A.G., and Millero F.J. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res. 34 (1987) 1733-1743
20. Edwards M., Licandro P., John A.W.G., and Johns D.G. Ecological status report: results from the CPR survey 2003/2004. SAHFOS Technical Report vol. 2 (2005) 1-6
21. Elzenga J.T.M., Prins H.B.A., and Stefels J. The role of extracellular carbonic anhydrase activity in inorganic carbon utilization of Phaeocystis globosa (Prymnesiophyceae): a comparison with other marine algae using the isotope disequilibrium technique. Limnol. Oceanogr. 45 (2000) 372-380
22. Falkowski P.G., Katz M.E., Knoll A.H., Quigg A., Raven J.A., Schofield O., and Taylor F.J.R. The evolution of modern eukaryotic phytoplankton. Science 305 (2004) 354-360
23. Fielding A.S., Turpin D.H., Guy R.D., Calvert S.E., Crawford D.W., and Harrison P.J. Influence of the carbon concentrating mechanism on carbon isotope discrimination by the marine diatom Thalassiosira pseudonana. Can. J. Bot. 76 (1998) 1098-1103
24. 2 levels. Glob. Biogeochem. Cycles 6 (1992) 185-198
25. Gibon Y., Blaesing O.E., Hannemann J., Carillo P., Höhne M., Hendriks J.H.M., Palacios N., Cross J., Selbig J., and Stitt M. A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes in enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16 (2004) 3304-3325
26. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56 (2005) 99-131
27. Gran G. Determinations of the equivalence point in potentiometric titrations of seawater with hydrochloric acid. Oceanol. Acta 5 (1952) 209-218
28. Granum E., Raven J.A., and Leegood R.C. How do marine diatoms fix 10 billion tonnes of inorganic carbon per year?. Can. J. Bot. 83 (2005) 898-908
29. Guillard R.R.L., and Ryther J.H. Studies of marine planktonic diatoms. Can. J. Microbiol. 8 (1962) 229-239
30. Hansen P.J. Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquat. Microb. Ecol. 28 (2002) 279-288
31. Hinga K.R. Effects of pH on coastal marine phytoplankton. Mar. Ecol. Prog. Ser. 238 (2002) 281-300
32. Hobson L.A. Paradox of the phytoplankton - an overview. Biol. Oceanogr. 6 (1988) 493-504
33. Hobson L.A., and McQuoid M.R. Temporal variations among planktonic diatom assemblages in a turbulent environment of the southern Strait of Georgia, British Columbia, Canada. Mar. Ecol. Prog. Ser. 150 (1997) 263-274
34. IPCC (Intergovernmental panel on climate change). Working Group 1 Report, The Physical Science Basis (2007). http://ipcc-wg1.ucar.edu/wg1/wg1-report.html http://ipcc-wg1.ucar.edu/wg1/wg1-report.html
35. Johnston A.M., Raven J.A., Beardall J., and Leegood R.C. Photosynthesis in a marine diatom. Nature 412 (2001) 40-41
36. Keeley J.E. Photosynthetic pathway diversity in a seasonal pool community. Funct. Ecol. 13 (1999) 106-118
37. Korb R.E., Saville P.J., Johnston A.M., and Raven J.A. Sources for inorganic carbon for photosynthesis by three marine species of marine diatom. J. Phycol. 33 (1997) 433-444
38. Kroth P.G., Chiovitti A., Gruber A., Martin-Jezequel V., Mock T., Parker M.S., Stanley M.S., Kaplan A., Caron L., Weber T., Maheswari U., Armbrust E.V., and Bowler C. A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE 3 1 (2008) e1426 10.1371/ journal.pone.0001426
39. Leggat W., Badger M.R., and Yellowlees D. Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol. 121 (1999) 1247-1255
40. 2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center (1998), Oak Ridge National Laboratory, U.S. Department of Energy
41. MacIntyre H.L., and Geider R.J. Regulation of RubisCO activity and its potential effect on photosynthesis during mixing in a turbid estuary. Mar. Ecol. Prog. Ser. 144 (1996) 247-264
42. MacIntyre H.L., Sharkey T.D., and Geider R.J. Activation and deactivation of ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) in three marine microalgae. Photosynth. Res. 51 (1997) 93-106
43. MacIntyre H.L., Kana T.M., and Geider J.R. The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci. 5 (2000) 12-16
44. Marshall H.G. Phytoplankton distribution along the Eastern Coast of the USA. Part 1. Phytoplankton composition. Mar. Biol. 38 (1976) 81-89
45. Marshall H.G. Phytoplankton distribution along the Eastern Coast of the USA. Part 2. Seasonal assemblages north of Cape Hatteras, North Carolina. Mar. Biol. 45 (1978) 203-208
46. Martin C.L., and Tortell P.D. Bicarbonate transport and extracellular carbonic anhydrase in marine diatoms. Physiol. Plant. 133 (2008) 106-116 10.1111/j.1399-3054.2008.01054.x
47. 4 pathway of marine diatoms. Plant Physiol. 146 (2008) 300-309
48. Mehrbach C., Culberson C., Hawley J., and Pytkovicz R. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18 (1973) 897-907
49. Mills D.K., and Wilkinson M. Photosynthesis and light in estuarine benthic microalgae. Bot. Mar. 29 (1986) 125-129
50. Mitchell C., and Beardall J. Inorganic carbon uptake by an Antarctic sea-ice diatom, Nitzschia frigida. Polar Biol. 16 (1996) 95-99
51. 2. Neth. J. Sea Res. 20 (1986) 211-223
52. Morel F.M.M., Cox E.H., Kraepiel A.M.L., Lane T.W., Milligan A.J., Schaperdoth I., Reinfelder J.A., and Tortell P.D. Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Funct. Plant Biol. 29 (2002) 301-308
53. Moroney J.V., and Ynalvez R.A. Proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. Eukaryotic Cell. 6 8 (2007) 1251-1259 10.1128/EC.00064-07
54. Nelson D.M., Tréguer P., Brzezinski M.A., Leynaert A., and Quéginer B. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob. Biogeochem. Cycles 9 (1995) 359-372
55. Nimer N.A., Iglesias-Rodriguez M.D., and Merrett M.J. Bicarbonate utilization by marine phytoplankton species. J. Phycol. 33 (1997) 625-631
56. Nimer N.A., Brownlee C., and Merrett M.J. Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiol. 120 (1999) 105-111
57. O'Leary M.H., Madhavan S., and Paneth P. Physical and chemical basis of carbon isotope fractionation in plants. Plant Cell Environ. 15 (1992) 1099-1104
58. Orr J.C., Fabry V.J., Aumont O., Bopp L., Doney S.C., Feely R.A., Gnanadesikan A., Gruber N., Ishida A., Joos F., Key R.M., Lindsay K., Maier-Reimer E., Matear R., Monfray P., Mouchet A., Najjar R.G., Plattner G.-K., Rodgers K.B., Sabine C.L., Sarmiento J.L., Schlitzer R., Slater R.D., Totterdell I.J., Weirig M.-F., Yamanaka Y., and Yool A. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437 (2005) 681-686
59. Palmqvist K., Yu J.-W., and Badger M.R. Carbonic anhydrase activity and inorganic carbon fluxes in low- and high-Ci cells of Chlamydomonas reinhardtii and Scenedesmus obliquus. Physiol. Plant. 90 (1994) 537-547
60. 2-concentrating mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J. Exp. Bot. 59 (2007) 1441-1461 10.1093/jxb/erm112
61. 2-concentrating mechanisms of the potentially toxic dinoflagellate Protoceratium reticulatum (Dinophyceae, Gonyaulacales). J. Phycol. 43 (2007) 693-701
62. Raven J.A. The vacuole: a cost-benefit analysis. Adv. Bot. Res. 25 (1997) 59-86
63. Raven J.A., and Lucas W.J. Energy costs of carbon acquisition. In: Lucas W.J., and Berry J.A. (Eds). Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms (1985), American Society of Plant Physiologists, Rockville, MD 305-324
64. Raven J.A., and Johnston A.M. Mechanisms of inorganic carbon acquisition in marine phytoplankton and their implications for the use of other resources. Limnol. Oceanogr. 36 (1991) 1701-1714
65. 4 photosynthesis in a marine diatom. Nature 407 (2000) 996-999
66. 4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol. 135 (2004) 2106-2111
67. Roberts K., Granum E., Leegood R.C., and Raven J.A. Carbon acquisition by diatoms. Photosynth. Res. 93 (2007) 79-88 10.1007/s11120-007-9172-2
68. Roberts K., Granum E., Leegood R.C., and Raven J.A. C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol. (2007) 10.1104/pp.107.102616
69. Rost B., Zondervan I., and Riebesell U. Light-dependant carbon isotope fractionation in the coccolithophorid Emiliania huxleyi. Limnol. Oceanogr. 47 (2002) 120-128
70. Rost B., Riebesell U., Burkhardt S., and Sültemeyer D. Carbon acquisition of bloom-forming marine phytoplankton. Limnol. Oceanogr. 48 (2003) 55-67
71. Rost B., Richter K.-U., Riebesell U., and Hansen P.J. Inorganic carbon acquisition in red tide dinoflagellates. Plant Cell Environ. 29 (2006) 810-822
72. Rost B., Riebesell U., and Sültemeyer D. Carbon acquisition of marine phytoplankton. Effect of photoperiod length. Limnol. Oceanogr. 51 (2006) 12-20
73. Rost B., Kranz S., Richter K.-U., and Tortell P. Isotope disequilibrium and mass spectrometric studies of inorganic carbon acquisition by phytoplankton. Limnol. Oceanogr. Methods 5 (2007) 328-337
74. Rotatore C., Colman B., and Kuzma M. The active uptake of carbon dioxide by the marine diatoms Phaeodactylum tricornutum and Cyclotella sp. Plant Cell Environ. 18 (1995) 913-918
75. 2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC6803. Funct. Plant Biol. 29 (2002) 123-129
76. Silverman D.N. Carbonic anhydrase. Oxygen-18 exchange catalyzed by an enzyme with rate contributing proton-transfer steps. Methods Enzymol. 87 (1982) 732-752
77. Smetacek V. Diatoms and the ocean carbon cycle. Protist 150 (1999) 25-32
78. Sültemeyer D. Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can. J. Bot. 76 (1998) 962-972
79. - transport in cyanobacteria. Plant Physiol. 116 (1998) 183-192
80. Tortell P.D., Martin C.L., and Corkum M.E. Inorganic carbon uptake and intracellular assimilation by subarctic Pacific assemblages. Limnol. Oceanogr. 51 (2006) 2102-2110
81. 2 sensitivity of Southern Ocean phytoplankton. Geophys. Res. Lett. 35 (2008) L04605 10.1029/2007GL032583
82. Trimborn S., Lundholm N., Thoms S., Richter K.-U., Krock B., Hansen P.J., and Rost B. Inorganic carbon acquisition in potentially toxic and non-toxic diatoms: the effect of pH-induced changes in the carbonate chemistry. Physiol. Plant. 133 (2008) 92-105 10.1111/j.1399-3054.2007.01038.x
83. Wolf-Gladrow D.A., and Riebesell U. Diffusion and reaction in the vicinity of plankton: a refined model for inorganic carbon transport. Mar. Chem. 59 (1997) 17-34
84. 2 concentration on growth and isotopic composition of marine phytoplankton. Tellus 51 (1999) 461-476
85. Wolfstein K., and Hartig P. The photosynthetic light dispensation system: application to microphytobenthic primary production. Mar. Ecol. Prog. Ser. 166 (1998) 63-71
86. 2 in Seawater: Equilibrium, Kinetics, Isotopes (2001), Elsevier Science, Amsterdam
87. 2. Geochim. Cosmochim. Acta 59 (1995) 107-114 [SS]