How do marine diatoms fix 10 billion tonnes of inorganic carbon per year?

Canadian Journal of Botany

Volumn 83, Issue 7, 2005, Pages 898-908

  Granum, Espen ^a   Raven, John A ^b   Leegood, Richard C ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

C4 photosynthesis; CO2 concentrating mechanism; Marine diatoms; Phosphoenolpyruvate carboxykinase; Phosphoenolpyruvate carboxylase

Indexed keywords

CELLS; ENZYMES; MARINE ENGINEERING; OCEANOGRAPHY; PHOTOSYNTHESIS; PLANTS (BOTANY);

C4 PHOTOSYNTHESIS; CO2-CONCENTRATING MECHANISM; MARINE DIATOMS; PHOSPHOENOLPYRUVATE CARBOXYKINASE; PHOSPHOENOLPYRUVATE CARBOXYLASE;

CARBON;

DIATOM; INORGANIC CARBON;

CARBON; CELLS; DIATOMS; ENZYMES; OCEANOGRAPHY; PHOTOSYNTHESIS; PLANTS;

BACILLARIOPHYTA; NITZSCHIA ALBA;

EID: 29144535365     PISSN: 00084026     EISSN: None     Source Type: Journal    
DOI: 10.1139/b05-077     Document Type: Conference Paper

References (77)

1. Apt, K.E., Zaslavkaia, L., Lippmeier, J.C., Lang, M., Kilian, O., Wetherbee, R., Grossman, A.R., and Kroth, P.G. 2002. In vivo characterization of diatom multipartite plastid targeting signals. J. Cell Sci. 115: 4061-4069.
2. Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H. et al. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science (Washington, D.C.), 306: 79-86.
3. 2-concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J. Exp. Bot. 54: 609-622.
4. 2 acquisition, concentration and fixation. In Photosynthesis: Physiology and metabolism. Edited by R.C. Leegood, T.D. Sharkey, and S. von Caemmerer. Kluwer, Dordrecht. pp. 369-397.
5. - fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol. Plant, 90: 529-536.
6. 2-concentrating mechanisms in algae. Can. J. Bot. 76: 1052-1071.
7. Beardall, J. 1989. Photosynthesis and photorespiration in marine phytoplankton. Aquat. Bot. 34: 105-130.
8. Beardall, J., Mukerji, D., Glover, H.E., and Morris, I. 1976. The path of carbon in photosynthesis by marine phytoplankton. J. Phycol. 12: 409-417.
9. 4 systems. Funct. Plant Biol. 29: 379-392.
10. 2 concentrations. Limnol. Oceanogr. 46: 1378-1391.
11. 4 acid decarboxylation in bundle sheath cells of Urochloa panicoides. Arch. Biochem. Biophys. 260: 187-199.
12. 4 pathway operation. Plant Physiol. 86: 1252-1256.
13. Cabello-Pasini, A., Smith, G.J., and Alberte, R.S. 2000. Phosphoenolpyruvate carboxykinase from the marine diatom Skeletonema costatum and the phaeophyte Laminaria setchellii. I. Isolation and biochemical characterization. Bot. Mar. 43: 559-568.
14. Cabello-Pasini, A., Swift, H., Smith, G.J., and Alberte, R.S. 2001. Phosphoenolpyruvate carboxykinase from the marine diatom Skeletonema costatum and the phaeophyte Laminaria setchellii. II. Immunological characterization and subcellular localization. Bot. Mar. 44: 199-207.
15. Chollet, R., Vidal, J., and O'Leary, M.H. 1996. Phosphoeno/pyruvate carboxylase: A ubiquitous, highly regulated enzyme in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 47: 273-298.
16. Colman, B., and Rotatore, C. 1988. Photosynthetic inorganic carbon uptake and accumulation in a freshwater diatom. J. Exp. Bot. 39: 1025-1032.
17. Colman, B., Huertas, I.A., Bhatti, S., and Dason, J.S. 2002. The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct. Plant Biol. 29: 261-270.
18. Coombs, J., and Volcani, B.E. 1968. Studies on the biochemistry and fine structure of silica shell formation in diatoms. Silicon-induced metabolic transients in Navicula pelliculosa (Bréb.) Hilse. Planta, 80: 264-279.
19. 2" used by PEP carboxykinase, carboxytransphosphorylase and pyruvate carboxylase. J. Biol. Chem. 243: 3857-3863.
20. 2" used by Ribulose diphosphate carboxylase. J. Biol. Chem. 244: 1081-1083.
21. Crawford, D.W., Lipsen, M.S., Purdie, D.A., Lohan, M.C., Statham, P.J., Whitney, F.A. et al. 2003. Influence of zinc and iron enrichments on phytoplankton growth in the northeastern subarctic Pacific. Limnol. Oceanogr. 48: 1583-1600.
22. Dalziel, K., and Londesborough, J.C. 1968. The mechanism of reductive carboxylation reactions. Carbon dioxide or bicarbonate as substrate of nicotinamide-adenine dinucleotide phosphate-linked isocitrate dehydrogenase and "malic" enzyme. Biochem. J. 110: 223-230.
23. Descolas-Gros, C., and Oriol, L. 1992. Variations in carboxylase activity in marine phytoplankton cultures. β-carboxylation in carbon flux studies. Mar. Ecol. Prog. Ser. 85: 163-169.
24. Dodge, J.D. 1973. The fine structure of algal cells. Academic Press, London.
25. Elzenga, J.T.M., Prins, H.B.A., and Stefels, J. 2000. The role of extracellular carbonic anhydrase activity in inorganic carbon utilization of Phaeocystis globosa (Prymnesiophyceae): a comparison with other marine algae using the isotopic disequilibrium technique. Limnol. Oceanogr. 45: 372-380.
26. Falkowski, P.G., and Raven, J.A. 1997. Aquatic photosynthesis. Blackwell Sciences, Maiden, Mass.
27. Franck, V.M., Bruland, K.W., Hutchins, D.A., and Brzezinski, M.A. 2003. Iron and zinc effect on silicic acid and nitrate uptake kinetics in three high-nutrient, low-chlorophyll (HNLC) regions. Mar. Ecol. Prog. Ser. 252: 15-33.
28. Gradmann, D., and Boyd, C. 1995. Membrane voltage of marine phytoplankton, measured in the diatom Coscinodiscus radiatus. Mar. Biol. 123: 645-650.
29. 2-concentrating mechanism in hornworts (Anthocerotophyta). Funct. Plant Biol. 29: 407-416.
30. Hatch, M.D., and Burnell, J.N. 1990. Carbonic anhydrase activity in leaves and its role in the first step of C4 photosynthesis. Plant Physiol. 93: 825-828.
31. Holdsworth, E.S., and Colbeck, J. 1976. The pattern of carbon fixation in the marine unicellular alga Phaeodactylum tricornutum. Mar. Biol. 38: 189-199.
32. Jenkins, C.D.L., Burnell, J.N., and Hatch, M.D. 1987. Form of inorganic carbon involved as a product and as an inhibitor of C-4 acid decarboxylases operating in C-4 photosynthesis. Plant Physiol. 85: 952-957.
33. Johnston, A.M. 1991. The acquisition of inorganic carbon by marine macroalgae. Can. J. Bot. 69: 1123-1132.
34. 4-like characteristics of the intertidal macroalga Ascophyllum nodosum (L) Le Jolis (Fucales, Phaeophyta). Phycologia, 26: 159-166.
35. Johnston, A.M., and Raven, J.A. 1996. Inorganic carbon accumulation by the marine diatom Phaeodactylum tricornutum. Eur. J. Phycol. 31: 285-290.
36. 4 photosynthesis in a diatom? Nature (London), 412: 40-41.
37. Korb, R.E., Saville, P.J., Johnston. A.M., and Raven J.A. 1997. Sources of inorganic carbon for photosynthesis by three species of marine diatom. J. Phycol. 33: 433-440.
38. Lang, M., Apt, K.E., and Kroth, P.G. 1998. Protein transport into "complex" diatom plastids utilizes two different targeting signals. J. Biol. Chem. 273: 30 973-30 978.
39. 2 concentrations. Protist, 149: 341-345.
40. Leegood, R.C., and Walker, R.P. 2003. Regulation and roles of phosphoenolpyruvate carboxykinase in plants. Arch. Biochem. Biophys. 414: 204-210.
41. Magnin, N.C., Cooley, B.A., Reiskind, J.B., and Bowes, G. 1997. Regulation and localization of key enzymes during the induction of Kranz-less, C-4-type photosynthesis in Hydrilla verticillata. Plant Physiol. 115: 1681-1689.
42. 2 in the marine diatom Phaeodactylum tricornutum. Plant Cell Environ. 24: 611-620.
43. McKay, R.M., and Gibbs, S.P. 1991. Composition and function of pyrenoids: cytochemical and immunocytochemical approaches. Can. J. Bot. 69: 1040-1052.
44. Morel, F.M.M., Cox, E.H., Kraepiel, A.M.L., Lane, T.W., Milligan, A.J., Schaperdoth, I., Reinfelder, J.R., and Tortell, P.D. 2002. Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Funct. Plant Biol. 29: 301-308.
45. 2-concentrating mechanism: comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas (Volvocales). Planta, 208: 365-372.
46. 14C incorporation in Skeletonema costatum (Greville) Cleve (Bacillarophyceae) as a function of light regime. Phycologia, 26: 262-269.
47. Mortain-Bertrand, A., Descolas-Gros, C., and Jupin, H. 1987b. Stimulating effect of light-to-dark transitions on carbon assimilation by a marine diatom. J. Exp. Mar. Biol. Ecol. 112: 11-26.
48. Mortain-Bertrand, A., Descolas-Gros, C., and Jupin, H. 1988a. Pathway of dark inorganic carbon fixation in two species of diatoms: influence of light regime and regulator factors on diel variations. J. Plankton Res. 10: 199-217.
49. Mortain-Bertrand, A., Descolas-Gros, C., and Jupin, H. 1988b. Growth, photosynthesis and carbon metabolism in the temperate marine diatom Skeletonema costatum adapted to low temperature and low photon-flux density. Mar. Biol. 100: 135-141.
50. Mukerji, D. 1980. Pyruvate-orthophosphate-dikinase and malic enzyme: their assays and significance in the photosynthetic carbon assimilation in some marine algae. Photosynthetica, 14: 517-522.
51. Price, N.M., Harrison, G.I., Hering, J.G., Hudson, R.J., Nirel, P.M.V., Palenik, B., and Morel, F.M.M. 1988-1989. Preparation and chemistry of the artificial algal culture medium Aquil. Biol. Oceanogr. 6: 443-461.
52. Raven, J.A. 1970. Exogenous inorganic carbon sources in plant photosynthesis. Biol. Rev. 45: 167-221.
53. Raven, J.A. 1997a. Inorganic carbon acquisition by marine autotrophs. Adv. Bot. Res. 27: 85-209.
54. 2-concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ. 20: 147-154.
55. Raven, J.A., and Beardall, J. 2003. Carbon acquisition mechanisms in algae: Carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In Photosynthesis in algae. Edited by A.W.D. Larkum, S.E Douglas, and J.A. Raven. Kluwer, Dordrecht. pp. 205-224.
56. 2. Plant Cell Environ. 22: 741-755.
57. Raven, J.A., Kubler, J.E., and Beardall, J. 2000. Put out the light, and then put out the light. J. Mar. Biol. Assoc. U.K. 80: 1-25.
58. 4 photosynthesis in a marine diatom. Nature (London), 407: 996-999.
59. 4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiol. 135: 2106-2111.
60. Reiskind, J.B., and Bowes, G. 1991. The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc. Natl. Acad. Sci. U.S.A. 88: 2883-2887.
61. 4-like alga. Plant Physiol. Suppl. 108: 89.
62. 2-concentrating mechanism in Hydrilla, a submersed monocot. Plant Cell Environ. 20: 211-220.
63. Rost, B., Riebesell, U., Burkhardt, S., and Sültemeyer, D. 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnol. Oceanogr. 48: 1042-1047.
64. 2 by the diatom Navicula pelliculosa. J. Exp. Bot. 43: 571-576.
65. Rotatore, C., Colman, B., and Kuzma, M. 1995. The active uptake of carbon dioxide by the marine diatoms Phaeodactylum tricornutum and Cyclotella sp. Plant Cell Environ. 18: 913-918.
66. Salvucci, M.E., and Bowes, G. 1981. Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes. Plant Physiol. 67: 335-340.
67. Salvucci, M.E., and Bowes, G. 1983. Two photosynthetic mechanisms mediating the low photorespiratory state in submersed aquatic angiosperms. Plant Physiol. 73: 488-496.
68. Satoh, D., Hiraoka, Y., Colman, B., and Matsuda, Y. 2001. Physiological and molecular biological characterization of intracellular carbonic anhydrase from the marine diatom Phaeodactylum tricornutum. Plant Physiol. 126: 1459-1470.
69. Tortell, P.D. 2000. Evolutionary and ecological perspectives on carbon acquisition in phytoplankton. Limnol. Oceanogr. 45: 744-750.
70. Tortell, P.D., Reinfelder, J.R., and Morel, F.M.M. 1997. Active uptake of bicarbonate by diatoms. Nature (London), 390: 243-244.
71. 3 leaves. Plant Cell Environ. 26: 1191-1197.
72. 2 pump. Photosynth. Res. 77: 191-207.
73. Voznesenskaya, E., Franceschi, V.R., Kiirats, O., Freitag, H., and Edwards, G.E. 2001. Kranz anatomy is not essential for terrestrial C4 photosynthesis. Nature (London), 414: 543-546.
74. 4 plants: its role and regulation. Aust. J. Plant Physiol. 24: 459-468.
75. Whitney, S.M., Baldet, P., Hudson, G.S., and Andrews, T.J. 2001. Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J. 26: 535-547.
76. Wingler, A., Walker, R.P., Chen, Z.-H., and Leegood, R.C. 1999. Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle-sheath of maize. Plant Physiol. 120: 539-545.
77. Wittpoth, C., Kroth, P.G., Weyrauch, K., Kowallik, K.V., and Strotmann, H. 1998. Functional characterization of isolated plastids from two marine diatoms. Planta, 206: 79-85.