The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae

Canadian Journal of Botany

Volumn 76, Issue 6, 1998, Pages 1052-1071

  Badger, Murray R ^a   Andrews, T John ^a   Whitney, S M ^a   Ludwig, Martha ^a   Yellowlees, David C ^b   Leggat, W ^b   Price, G Dean ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

Author keywords

Algae; Aquatic photosynthesis; Carbonic anhydrase; CO2 concentrating mechanism; Inorganic carbon; Pyrenoids; Ruhisco

Indexed keywords

ALGA; CARBON DIOXIDE; CARBON DIOXIDE CONCENTRATING MECHANISM; CHLOROPLAST; ENZYME KINETICS; OXYGEN; PHOTOSYNTHESIS; PYRENOID; RIBULOSEBISPHOSPHATE CARBOXYLASE; THYLAKOID;

ALGAE; EMBRYOPHYTA; EUKARYOTA;

EID: 0032410294     PISSN: 00084026     EISSN: None     Source Type: Journal    
DOI: 10.1139/b98-074     Document Type: Article

References (107)

1. 2 concentrating mechanisms in microalgae and cyanobacteria (review). FEMS Microbiol. Rev. 39: 215-233.
2. Axelsson, L., Ryberg, H., and Beer, S. 1995. Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca. Plant Cell Environ. 18: 439-445.
3. 2-concentrating mechanism in aquatic phototrophs. In The biochemistry of plants: a comprehensive treatise. Vol. 10. Photosynthesis. Edited by M.D. Hatch and N.K. Boardman. Academic Press, San Diego, Calif, pp. 219-274.
4. 2 concentrating mechanisms. In Progress in photosynthesis research. Vol. III. Edited by J. Biggins. Martinus Nijhoff Publishers, Dordrecht, The Netherlands, pp. 601-609.
5. Badger, M.R., and Price, G.D. 1989. Carbonic anhydrase activity associated with the cyanobacterium Synechococcus PCC7942. Plant Physiol. 89: 51-60.
6. 2 concentrating mechanism in cyanobacteria and microalgae. Physiol. Plant. 84: 606-615.
7. 2) form of RuDP carboxylase, having high RuDP oxygenase activity at physiological pH. In Proceedings of the 3rd International Conference on Photosynthesis. Edited by M. Avron. Elsevier Scientific Publishing Co., Amsterdam, The Netherlands, and The Weizmann Institute of Science. Rehovot, Israel, pp. 1421-1429.
8. Badger, M.R., Kaplan, A., and Berry, J.A. 1980. Internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a carbon dioxide concentrating mechanism. Plant Physiol. 66: 407-413.
9. - accumulation and photosynthesis in the cyanobacterium Svnechococcus sp. Theoretrial predictions and experimental observations. Plant Physiol. 77: 465-471.
10. 2 accumulation by Chlorella saccharophila (chlorophyceae) at low external pH: evidence for active-transport of inorganic carbon at the chloroplast envelope. J. Phycol. 17: 371-373.
11. Beardall, J. 1989. Photosynthesis and photorespiration in marine phytoplankton. Aquat. Bot. 43: 104-130.
12. 2 kinetics. Plant Physiol. 94: 1542-1546.
13. Bermanfrank, I., and Erez, J. 1996. Inorganic carbon pools in the bloom-forming dinoflagellate Peridinium gatunense. Limnol. Oceanogr. 41: 1780-1789.
14. - utilization and repression of photorespiration in protoplasts and thalli of three species of Ulva (Chlorophyta). J. Phycol. 29: 166-173.
15. Bold, H.C., and Wynne, M.J. 1985. Introduction to the algae. Structure and reproduction. Prentice-Hall, Inc., Edgewood Cliffs, N.J.
16. 2 [carbon dioxide] concentration. Plant Physiol. 75: 919-923.
17. Brechignac, F., and Andre, M. 1985. Oxygen uptake and photosynthesis of the red macroalga, Chondrus crispus, in seawater. Effects of oxygen concentration. Plant Physiol. 78: 545-550.
18. Burns, B.D., and Beardall, J. 1987. Utilization of inorganic carbon by marine microalgae. J. Exp. Mar. Biol. Ecol. 107: 75-86.
19. Canvin, D.T., Berry, J.A., Badger, M.R., Fock, H., and Osmond, C.B. 1980. Oxygen exchange in leaves in the light. Plant Physiol. 66: 302-307.
20. Caperon, J., and Smith, D.F. 1978. Photosynthetic rates of marine algae as a function of inorganic carbon concentration. Limnol. Oceanogr. 23: 704-708.
21. 2 specificity of ribulose-bisphosphate carboxylase/oxygenase in a temperature-sensitive chloroplast mutant of Chlamydomonas. Proc. Natl. Acad. Sci. U.S.A., 85: 4696-4699.
22. Colman, B., and Gehl, K.A. 1983. Physiological characteristics of photosynthesis in Porphyridium cruentum: evidence for bicarbonate transport in a unicellular red alga. J. Phycol. 19: 216-219.
23. Colman, B., and Rotatore, C. 1988. Uptake and accumulation of inorganic carbon by a freshwater diatom. J. Exp. Bot. 39: 1025-1032.
24. Colman, B., and Rotatore, C. 1995. Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant Cell Environ. 18: 919-924.
25. Cook, C.M., and Colman, B. 1987. Some characteristics of photosynthetic inorganic carbon uptake of a marine macrophytic red alga (technical note). Plant Cell Environ. 10: 275-278.
26. Couture, M., Chamberland, H., St. Pierre, B., Lafontaine, J., and Guertin, M. 1994. Nuclear genes encoding chloroplast hemoglobins in the unicellular green alga Chlamydomonas eugametos. Mol. Gen. Genet. 243: 185-97.
27. De Luca, P., Taddei, R., and Varano, L. 1978. Cyanidioschyzon merolae: a new alga of thermal acidic environments. Webbia, 33: 37-44.
28. Delwiche, C.F., and Palmer, J.D. 1996. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 13: 873-882.
29. Dixon, G.K., and Merrett, M.J. 1988. Bicarbonate utilization by the marine diatom Phaeodactylum tricornutum Bohlin. New Phytol. 109: 47-51.
30. Dodge, J. 1973. The pyrenoid. In The fine structure of algal cells. Edited by J. Dodge. Academic Press, London, U.K. pp. 105-124.
31. Dong, L.F., Nimer, N.A., Okus, E., and Merrett, M.J. 1993. Dissolved inorganic carbon utilization in relation to calcite production in Emiliania huxleyi (Lohmann) Kamptner. New Phytol. 123: 679-684.
32. Ettl, H. 1978. Xanthophyceae. In Susswasserflora von Mitteleuropa. Edited by H. Ettl, J. Gerloff, and H. Heynig. Vol. 1. Gustav Fischer, Stuttgart, Germany, pp. 1-530.
33. Ettl, H. 1983. Chlorophyta I. In Susswasserflora von Mitteleuropa. Edited by H. Ettl, J. Gerloff, and D. Mollenhauer. Gustaff Fischer Verlag, Stuttgart, Germany, pp. 1-807.
34. Furbank, R.T., Badger, M.R., and Osmond, C.B. 1982. Photosynthetic oxygen-exchange in isolated cells and chloroplasts of C3 plants. Plant Physiol. 70: 927-931.
35. Garbary, D.J., Hansen, G.I., and Scagel, R.F. 1980. A revised classification of the Bangiophyceae (Rhodophyta). Nova Hedwigia, 33: 145-166.
36. Garcia Sanchez, M.J., Fernandez, J.A., and Niell, X. 1994. Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta, 194: 55-61.
37. 2 affinity of Chlorella saccharophila. J. Exp. Bot. 38: 1203-1210.
38. Gehl, K.A., Colman, B., and Sposato, L.M. 1990. Mechanism of inorganic carbon uptake in Chlorella saccharophila: the lack of involvement of carbonic anhydrase. J. Exp. Bot. 41: 1385-1391.
39. 2, and light on photosynthesis and photorespiration in wheat. Plant Physiol. 66: 1032-1036.
40. Giordano, M., and Maberly, S.C. 1989. Distribution of carbonic anhydrase in British marine macroalgae. Oecologia, 81: 534-539.
41. Griffiths, D.J. 1970. The pyrenoid. Bot. Rev. 36: 29-58.
42. Gutteridge, S., Sigal, I., Thomas, B., Arentzen, R., Cordova, A., and Lorimer, G. 1984. A site-specific mutation within the active-site of ribulose-1,5-bisphosphate carboxylase of Rhodospirillum rubrum. EMBO J. 3: 2737-2743.
43. Haglund, K., Bjork, M., Ramazanov, Z., Garcia Reina, G., and Pedersen, M. 1992a. Role of carbonic anhydrase in photosynthesis and inorganic-carbon assimilation in the red alga Gracilaria tenuistipitata. Planta, 187: 275-281.
44. Haglund, K., Ramazanov, Z., Mtolera, M., and Pedersen, M. 1992b. Role of external carbonic anhydrase in light-dependent alkalization by Fucus serratus L., and Laminaria saccharina (L.) Lamour. (Phaeophyta). Planta, 188: 1-6.
45. Hatch, M.D. 1987. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta, 895: 81-106.
46. - uptake. Mar. Biol. 112: 697-700.
47. Johnston, A.M. 1991. The acquisition of inorganic carbon by marine macroalgae. Can. J. Bot. 69: 1123-1132.
48. 2 on the photosynthetic physiology of Fucus serrants. Br. Phycol. J. 25: 75-82.
49. Jordan, D.B., and Chollet, R. 1985. Subunit dissociation and reconstitution of ribulose-1,5-bisphosphate carboxylase from Chromatium vinosum. Arch. Biochem. Biophys. 236: 487-496.
50. Jordan, D.B., and Ogren, W.L. 1981. Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature (London), 291: 513-515.
51. Jordan, D.B., and Ogren, W.L. 1983. Species variation in kinetic-properties of ribulose 1,5-bisphosphate carboxylase oxygenase. Arch. Biochem. Biophys. 227: 425-433.
52. 2 specificity of ribulose bisphosphate carboxylase-oxygenase. Aust. J. Plant Physiol. 21: 449-461.
53. 2 concentration. Planta, 149: 219-226.
54. Kaplan, A., Schwarz, R., Lieman Hurwitz, J., and Reinhold, L. 1991. Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol. 97: 851-855.
55. Kerby, N.W., and Raven, J.A. 1985. Transport and fixation of inorganic carbon by marine algae. Adv. Bot. Res. 11: 71-123.
56. Kuppers, U., and Weidner, M. 1980. Seasonal-variation of enzyme-activities in Laminaria hyperborea. Planta, 148: 222-230.
57. Lilley, R.M., and Walker, D.A. 1975. Carbon dioxide assimilation by leaves, isolated chloroplasts, and RuDP carboxylase from spinach. Plant Physiol. 55: 1087-1092.
58. - by aquatic plants. Annu. Rev. Plant Physiol. 34: 71-104.
59. 2. J. Exp. Bot. 47: 1951-1956.
60. McKay, R.M.L., and Gibbs, S.P. 1991. Composition and function of pyrenoids: cytochemical and immunocytochemical approaches. Can. J. Bot. 69: 1040-1052.
61. - use by the inorganic carbon level in Porphyra leucosticta Thur in le Jolis (Rhodophyta). Planta, 201: 319-325.
62. Merrett, M.J. 1991. Inorganic carbon transport in some marine microalgal species. Can. J. Bot. 69: 1032-1039.
63. Merrett, M.J., Nimer, N.A., and Dong, L.F. 1996. The utilization of bicarbonate ions by the marine microalga Nannochloropsis oculata (Droop) Hibberd. Plant Cell Environ. 19: 478-484.
64. 2 transport in cyanobacteria. Can. J. Bot. 69: 925-935.
65. Morell, M.K., Paul, K., Kane, H.J., and Andrews, T.J. 1992. Rubisco: maladapted or misunderstood? Aust. J. Bot. 40: 431-441.
66. Morell, M.K., Paul, K., O'Shea, N.J., Kane, H.J., and Andrews, T.J. 1994. Mutations of an active site threonyl residue promote b elimination and other side reactions of the enediol intermediate of the ribulose bisphosphate carboxylase reaction. J. Biol. Chem. 269: 8091-8098.
67. Moroney, J.V., Kitayama, M., Togasaki, R.K., and Tolbert, N.B. 1987. Evidence for inorganic carbon transport by intact chloroplasts of Chlamydomonas reinhardtii (technical note). Plant Physiol. 83: 460-463.
68. Munoz, J., and Merrett, M.J. 1988. Inorganic-carbon uptake by a small-celled strain of Stichococcus bacilaris. Planta, 175: 460-464.
69. Nimer, N.A., Dixon, G.K., and Merrett, M.J. 1992. Utilization of inorganic carbon by the coccolithophorid Emiliania huxleyi (Lohmann) Kamptner. New Phytol. 120: 153-158.
70. Nimer, N.A., Guan, Q., and Merrett, M.J. 1994. Extra- and intracellular carbonic anhydrase in relation to culture age in a high-calcifying strain of Emiliania huxleyi Lohman. New Phytol. 126: 601-607.
71. Okazaki, M., Aruga, S., and Okamura, Y. 1992. Role of carbonic anhydrase in photosynthesis of unicellular marine algae coccolithophorids (Haptophyta). In Research in photosynthesis. Edited by N. Murata. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 783-786.
72. 2 and light responses of Coccomyxa, Chlamydomonas reinhardtii and barley protoplasts. Plant Cell Environ. 17: 65-72.
73. i cells of Chlamydomonas reinhardtii and Scenedesmus obliguus. Physiol. Plant. 90: 537-547.
74. 2 cells of Chlamydomonas reinhardtii. Planta, 197: 352-361.
75. 2 uptake in the cyanobacterium Synechococcus PCC7942 without apparent inhibition of internal carbonic anhydrase activity. Plant Physiol. 89: 37-43.
76. 2-dependent photosynthesis in the cyanobacterium Synechococcus PCC7942. Plant Physiol. 89: 44-50.
77. 2 concentrating mechanism. Plant Physiol. 91: 505-513.
78. Radmer, R.J., and Ollinger, O. 1978. Kinetics and apparent Km of oxygen cycle under conditions of limiting carbon dioxide fixation. Plant Physiol. 61: 915-917.
79. Radmer, R.J., and Ollinger, O. 1980. Light-driven uptake of oxygen, carbon-dioxide, and bicarbonate by the green-alga Scenedesmus. Plant Physiol. 65: 723-729.
80. 2-concentrating mechanisms: a direct role for thylakoid lumen acidification. Plant Cell Environ. 20: 147-154.
81. Raven, J.A., Johnston, A.M., and MacFarlane, J.J. 1990. Carbon metabolism. In Biology of the red algae. Edited by K.M. Cole and R.G. Sheath. Cambridge University Press, Cambridge, U.K. pp. 171-202.
82. Read, B.A., and Tabita, F.R. 1994. High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial Rubisco containing "algal" residue modifications. Arch. Biochem. Biophys. 312: 210-218.
83. 2 by the diatom Navicula pelliculosa. J. Exp. Bot. 43: 571-576.
84. Seemann, J.R., Badger, M.R., and Berry, J.A. 1984. Variations in the specific activity of ribulose-1,5-bisphosphate carboxylase between species utilizing differing photosynthetic pathways. Plant Physiol. 74: 791-794.
85. Sekino, K., and Shiraiwa, Y. 1994. Accumulation and utilization of dissolved inorganic carbon by a marine unicellular coccolithophorid, Emiliania huxleyi. Plant Cell Physiol. 35: 353-361.
86. Sekino, K., Kobayashi, H., and Shiraiwa, Y. 1996. Role of coccoliths in the utilization of inorganic carbon by a marine unicellular coccolithophorid, Emiliania huxleyi: a survey using intact cells and protoplasts. Plant Cell Physiol. 37: 123-127.
87. 2-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes. Planta, 198: 6-16.
88. Smith, B.C., and Griffiths, H. 1996b. A pyrenoid-based carbon-concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta. 200: 203-212.
89. Smith, R.G., and Bidwell, R.G.S. 1987. Carbonic anhydrase-dependent inorganic carbon uptake by the red macroalga, Chondrus crispus. Plant Physiol. 83: 735-738.
90. Smith, R.G., and Bidwell, R.G.S. 1989. Mechanism of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol. 89: 93-99.
91. Spalding, M.H. 1989. Photosynthesis and photorespiration in fresh-water green algae. Aquat. Bot. 34: 181-209.
92. Stemler, A. 1985. Carbonic anhydrase: molecular insights applied to photosystem II research in thylakoid membranes. In Inorganic carbon uptake by aquatic photosynthetic organisms. Edited by W.J. Lucas and J.A. Berry. American Society of Plant Physiologists, Rockville, Md. pp. 377-387.
93. 2 in suspensions of carbonic anhydrase-loaded plasma-membrane vesicles. Planta, 200: 358-368.
94. 2 concentrations. Planta, 176: 256-260.
95. 2-enriched air. Plant Physiol. 81: 372-375.
96. Sültemeyer, D., Biehler, K., and Fock, H. 1993. Evidence for the contribution of pseudocyclic photophosphorylation to the energy requirement of the mechanism for concentrating inorganic carbon in Chlamydomonas. Planta, 189: 235-242.
97. Surif, M.B., and Raven, J.A. 1989. Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): ecological and taxonomic implications. Oecologia, 78: 97-105.
98. 2 fixation in purple bacteria. In Anoxygenic photosynthetic bacteria. Edited by R.E. Blankenship, M.T. Madigan, and C.T. Bauer. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 885-914.
99. - to carbonic anhydrase in Chlorella vulgaris (UTEX 263). Plant Physiol. 80: 997-1001.
100. Tu, C.K., Spiller, H., Wynns, G.C., and Silverman, D.N. 1987. Carbonic-anhydrase and the uptake of inorganic carbon by Synechococcus sp. (UTEX-2380). Plant Physiol. 85: 72-77.
101. 2 fixation. Biochem. Biophys. Res. Commun. 233: 568-571.
102. 2 concentrating mechanism in a starch-less mutant of Chlamydomonas reinhardtii. Physiol. Plant. 98: 798-802.
103. von Caemmerer, S., Evans, J.R., Hudson, G.S., and Andrews, T.J. 1994. The kinetics of ribulose-1,5-bisphosphate carboxylase/ oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta, 195: 88-97.
104. Watson, G.M.F., and Tabita, F.R. 1996. Regulation, unique gene organization, and unusual primary structure of carbon fixation genes from a marine phycoerythrin-containing cyanobacterium. Plant Mol. Biol. 32: 1103-1115.
105. Watson, G.M.F., and Tabita, F.R. 1997. Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: a molecule for phylogenetic and enzymological investigation. FEMS Microbiol. Lett. 146: 13-22.
106. Whitney, S.M., and Yellowlees, D. 1995. Preliminary investigations into the structure and activity of ribulose bisphosphate carboxylase from two photosynthetic dinoflagellates. J. Phycol. 31: 138-146.
107. Zenvirth, D., Volokita, M., and Kaplan, A. 1985. Photosynthesis and inorganic carbon accumulation in the acidophilic alga Cvanidioschyzon merolae. Plant Physiol. 77: 237-239.