Advertisement

CO2 Concentrating Mechanisms

  • Sue G. Bartlett
  • Mautusi Mitra
  • James V. Moroney
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 23)

Many photosynthetic organisms, from bacteria to algae to higher plants, have mechanisms for accumulating inorganic carbon in the vicinity of ribulose-1,5-bisphosphate carboxylase/oxygenase at the site of photosynthesis and thus minimizing photorespiration and increasing net carbon fixation. In this review components of carbon dioxide concentrating mechanisms (CCMs) are described. The best characterized of these systems, the CCM found in some cyanobacteria, is used as a paradigm. The CCM found in microscopic green algae is then described, with emphasis on Chlamydomonas reinhardtii. The CCMs utilized by higher plants that carry out C4 or Crassulacean acid metabolism are then reviewed. Finally, efforts to introduce a CCM into C3 plants using genetic engineering, the effects of the CCM on the global carbon cycle, and important research directions in this field are presented.

Keywords

Carbonic Anhydrase Crassulacean Acid Metabolism Bundle Sheath Cell Chloroplast Envelope Marine Cyanobacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alber BE and Ferry JG (1994) A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci USA 91: 6909-6913PubMedGoogle Scholar
  2. Badger MR (1987) The CO2 concentrating mechanism in aquatic phototrophs. In: Hatch MD, Boardman NK (eds) The Bio-chemistry of Plants: A Comprehensive Treatise, Vol 10, Pho-tosynthesis, pp 219-274 Academic Press, San DiegoGoogle Scholar
  3. Badger MR (2003) The roles of carbonic anhydrases in photo-synthetic CO2 concentrating mechanisms. Photosynth Res 77: 83-94PubMedGoogle Scholar
  4. Badger MR and Price GD (1992) The CO2 concentrating mecha-nism in cyanobacteria and microalgae. Physiol Plant 84: 606-615Google Scholar
  5. Badger MR and Price GD (1994) The role of carbonic anhydrase in photosynthesis. Annu Rev Plant Physiol and Plant Mol Biol 45: 369-392Google Scholar
  6. Badger MR and Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54: 609-622PubMedGoogle Scholar
  7. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W and Price GD (1998) The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CCMs in the algae. Can J Bot 76:1052-1071Google Scholar
  8. Badger MR, Hanson DT and Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29: 161-173Google Scholar
  9. Behrenfeld MJ, Bale AJ, Kolber ZS, Aiken J and Falkowski, PG (1996) Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383:508-510Google Scholar
  10. Berry J, Boynton JE, Kaplan A and Badger MR (1976) Growth and photosynthesis of Chlamydomonas reinhardtii as a function of CO2 concentration. Carnegie I Wash 75: 423-432Google Scholar
  11. Black CC (1973) Photosynthetic carbon fixation in relation to net CO2 uptake. Annu Rev Plant Physiol 24: 253-286Google Scholar
  12. Bonfil DJ, Ronen-Tarazi M, Sultemeyer D, Lieman-Hurwitz J, Schatz D and Kaplan A (1998) A putative HCO3 transporter in the cyanobacterium Synechococcus spStrain PCC 7942. FEBS Lett 430: 236-240PubMedGoogle Scholar
  13. Borkhsenious ON, Mason CB and Moroney JV (1998) The in-tracellular localization of ribulose-1,5-bisphosphate carboxy-lase/oxygenase in Chlamydomonas reinhardtii. Plant Physiol 116: 1585-1591PubMedGoogle Scholar
  14. Bowes G, Rao SK, Estavillo GM and Reiskind JB (2002) C4 mechanisms in aquatic angiosperms: comparisons with ter-restrial C4 systems. Funct Plant Biol 29: 379-392Google Scholar
  15. Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, Murdoch R, Bakker DCE, Bowie AR, Buesseler KO, Chang H, Charette M, Croot P, Downing K, Frew R, Gall M, Hadfield M, Hall J, Harvey M, Jameson G, Laroche J, Liddicoat M, Ling R, Mal-donado MT, Mckay RM, Nodder S, Pickmere S, Pridmore R, Rintoul S, Safi K, Sutton P, Strzepek R, Tanneberger K, Turner S, Waite A and Zeldis J (2000) A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertil-ization. Nature 407: 695-702PubMedGoogle Scholar
  16. Bracey MH, Christiansen J, Tovar P, Cramer SP and Bartlett SG (1994) Spinach carbonic anhydrase: investigation of the zinc-binding ligands by site-directed mutagenesis, elemental analysis and EXAFS. Biochem 33: 13126-13131Google Scholar
  17. Burnell JN and Hatch MD (1988) Low bundle sheath carbonic anhydrase is apparently essential for effective C4 pathway op-eration. Plant Physiol 86: 1252-1256PubMedGoogle Scholar
  18. Burnell JN, Gibbs MJ and Mason JG (1990) Spinach chloroplas-tic carbonic anhydrase-nucleotide sequence analysis of cDNA. Plant Physiol 92: 37-40PubMedGoogle Scholar
  19. Burnell JN, Ludwig M and Sugiyama T (1999) Accession num-bers T02079 and T02080Google Scholar
  20. Cannon GC, Heinhorst S, Bradburne CE and Shively JM (2002) Carboxysome genomics: a status report. Funct Plant Biol 29: 175-182Google Scholar
  21. Chen Z-Y, Lavigne LL, Mason CB and Moroney JV (1997) Cloning and overexpression of two cDNAs encoding the low CO2 -inducible chloroplast envelope protein LIP-36 from Chlamydomonas reinhardtii. Plant Physiol 114: 265-273PubMedGoogle Scholar
  22. Chirica L, Elleby B and Lindskog S (2001) Cloning, expression and some properties of α-carbonic anhydrase from Helicobac-ter pylori. Biochim Biophys Acta 1544: 55-63PubMedGoogle Scholar
  23. Chollet R, Vidal J and O’Leary MH (1996) Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 273-298PubMedGoogle Scholar
  24. Colman B, Huertas IE, Bhatti S and Dason JS (2002) The diver-sity of inorganic carbon acquisition mechanisms in eukaryotic algae. Funct Plant Biol 29: 261-270Google Scholar
  25. Cushman JC and Bohnert HJ (1997) Molecular genetics of Cras-sulacean acid metabolism. Plant Physiol 113: 667-676PubMedGoogle Scholar
  26. Day DA and Siedow JN (2000) Respiration and photorespiration. In: Buchanan B, Gruissem W and Jones R (eds) Biochemistry and Molecular Biology of Plants, pp 676-728. Amer Soc Plant Physiol, Rockville, MDGoogle Scholar
  27. Dodd AN, Borland AM, Haslam RP, Griffiths H and Maxwell K (2002) Crassulacean acid metabolism: plastic, fantastic. J Exp Bot 53: 569-580PubMedGoogle Scholar
  28. Elleby B, Chirica LC, Tu C, Zeppezauer M and Lindskog S (2001) Characterization of carbonic anhydrase from Neisseria gon-orrhoeae. Eur J Biochem 268: 1613-1619PubMedGoogle Scholar
  29. Eriksson M, Karlsson J, Ramazanov Z, Gardestr öm P and Samuelsson G (1996) Discovery of an algal mitochondrial car-bonic anhydrase: molecular cloning and characterization of a low-CO2 induced polypeptide in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 93: 12031-12034PubMedGoogle Scholar
  30. Falkowski P, Barber RT and Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary productivity. Science 281: 200-206PubMedGoogle Scholar
  31. Fawcett TW, Browse JA, Volokita M and Bartlett SG (1990) Spinach carbonic-anhydrase primary structure deduced from the sequence of a cDNA clone. J Biol Chem 265: 5414-5417PubMedGoogle Scholar
  32. Fett JP and Coleman JR (1994) Characterization and expression of two cDNAs encoding carbonic-anhydrase in Arabidopsis thaliana. Plant Physiol 105: 707-713PubMedGoogle Scholar
  33. Field CB, Behrenfeld MJ, Randerson JT and Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and Oceanic components. Science 281: 237-240PubMedGoogle Scholar
  34. Fisher M, Gokhman I, Pick U and Zamir A (1996) A salt-resistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem 271:17718-17723PubMedGoogle Scholar
  35. Friedberg D, Jager KM, Kessel M, Silman NJ and Bergman B (1993) Rubisco but not Rubisco activase is clustered in the carboxysomes of the cyanobacterium Synechococcus PCC 7942: mud-induced carboxysomeless mutants. Mol Microbiol 9: 1193-1201PubMedGoogle Scholar
  36. Fujiwara S, Fukuzawa H, Tachiki A and Miyachi S (1990) Struc-ture and differential expression of two genes encoding car-bonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 9779-9783PubMedGoogle Scholar
  37. Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisio-Sese ML and Miyachi S (1990) cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii- regulation by environmental CO2 concentration. Proc Natl Acad Sci USA 87: 4383-4387PubMedGoogle Scholar
  38. Fukuzawa H, Suzuki E, Komukai Y and Miyachi S (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Syne-chococcus PCC 7942. Proc Natl Acad Sci USA 89: 4437-4441PubMedGoogle Scholar
  39. Funke RP, Kovar JL and Weeks DP (1997) Intracellular carbonic anhydrase is essential to photosynthesis in Chlamydomonas reinhardtii at atmospheric levels of CO2 . Plant Physiol 114: 237-244PubMedGoogle Scholar
  40. Gibbs SP (1962) The ultrastructure of the pyrenoids of green algae. J Ultrastructure Res 7: 262-272Google Scholar
  41. G ötz R, Gnann A and Zimmermann FK (1999) Deletion of the carbonic anhydrase-like gene NCE103 of the yeast Saccha-romyces cerevisiae causes an oxygen-sensitive growth defect. Yeast 15: 855-864Google Scholar
  42. Goyal A and Tolbert NE (1989) Uptake of inorganic carbon by isolated chloroplasts from Dunaliella tertiolecta. Plant Physiol 89:1264-1269PubMedGoogle Scholar
  43. Hanson DT, Franklin LA, Samuelsson G and Badger MR (2003) The Chlamydomonas reinhardtii cia3 mutant lacking a thy-lakoid lumen-localized carbonic anhydrase is limited by CO2 utilization by Rubisco and not PSII function in vivo. Plant Physiol 132:2267-2275PubMedGoogle Scholar
  44. Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81-106Google Scholar
  45. Hausler RE, Hirsch H-J, Kreuzaler F and Peterhansel C (2002) Overexpression of C4-cycle enzymes in transgenic C3 plants: a biotechnological approach to improve C3-photosynthesis. J Exp Bot 53: 591-607PubMedGoogle Scholar
  46. Heazlewood JL, Tonti-Filippini JS, Gout AM, Day DA, Whelan J and Millar AH (2004) Experimental analysis of the mitochon-drial proteome highlights signaling and regulatory compo-nents, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16: 241-256PubMedGoogle Scholar
  47. Hewett-Emmett D and Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the α-, ß-, and γ-carbonic anhydrase gene families. Mol Phylogene and Evol 5: 50-77Google Scholar
  48. Honegger R (1991) Functional aspects of the lichen symbio-sis. Annu Rev Plant Physiol and Plant Mol Biol 42: 553-578Google Scholar
  49. Im CS, Zhang Z, Shrager J, Chang CW and Grossman AR (2003) Analysis of light and CO2 regulation in Chlamydomonas rein-hardtii using genome-wide approaches. Photosyn Res 75: 111-125PubMedGoogle Scholar
  50. Jordan DB and Ogren WL (1981) Species variation in the speci-ficity of ribulose bisphosphate carboxylase-oxygenase. Nature 291: 513-515Google Scholar
  51. Jordan DB and Ogren WL (1983) Species variation in the kinetic properties of ribulose 1,5-bisphosphate carboxylase/ oxyge-nase. Arch Biochem Biophys 274: 425-433Google Scholar
  52. Kaplan A and Reinhold L (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Molecular Biol 50: 539-570Google Scholar
  53. Kaplan A, Schwarz R, Lieman-Hurwitz J and Reinhold L (1994) Physiological and molecular studies on the response of cyanobacteria to changes in the ambient inorganic carbon concentration. In: Bryant D (ed) Molecular biology of the Cyanobacteria, pp 469-485. Kluwer Academic Pub, Dordecht, The NetherlandsGoogle Scholar
  54. Karlsson J, Hiltonen T, Husic HD, Ramazanov Z and Samuelsson G (1995) Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 109: 533-539PubMedGoogle Scholar
  55. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV and Samuelsson G (1998) A novel alpha-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2 . EMBO J 17: 1208-1216PubMedGoogle Scholar
  56. Keys AJ (1986) Rubisco: its role in photorespiration. Phil Trans R Soc Lon Ser B 313: 325-336Google Scholar
  57. Khalifah RG (1971) The carbon dioxide hydration activity of carbonic anhydrase, Stop-flow kinetic studies on the native human isoenzymes B and C. J Biol Chem 246: 2561-2573PubMedGoogle Scholar
  58. Kimber MS and Pai EF (2000) The active site architecture of Pisum sativum β-carbonic anhydrase is a mirror image of that of α-carbonic anhydrases. EMBO J 19: 1407-1418PubMedGoogle Scholar
  59. Kisker C, Schindelin H, Alber BE, Ferry JG and Rees DC (1996) A left-handed beta-helix revealed by the crystal structure of a carbonic anhydrase from the archaeon Methanosarcina thermophila, EMBO J 15: 2323-2330PubMedGoogle Scholar
  60. Ku MSB, Kano Murakami Y and Matsuoka M (1996) Evolution and expression of C4 photosynthesis genes. Plant Physiol 111: 949-957PubMedGoogle Scholar
  61. Kuchitsu K, Tsuzuki M and Miyachi S (1991) Polypeptide com-position of the pyrenoid and its regulation by CO2 concentra-tion in unicellular green algae. Can J Bot 69: 1062-1069Google Scholar
  62. Lane TW, Saito MA, George GN, Pickering IJ, Prince RC and Morel FMM (2005) A cadmium enzyme from a marine diatom. Nature 435: 42PubMedGoogle Scholar
  63. Leegood RC (2002) C4 photosynthesis: principles of CO2 con-centration and prospects for its introduction into C3 plants. J Exp Bot 53: 581-590PubMedGoogle Scholar
  64. Lieman-Hurwitz J, Rachmilevitch S, Mittler R, Marcus Y and Kaplan A (2003) Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO3 accumulation in cyanobacteria. Plant Biotech J 1: 43-50Google Scholar
  65. Lindskog S (1997) Structure and mechanism of carbonic anhy-drase. Pharmacol Ther 74: 1-20PubMedGoogle Scholar
  66. Ludwig M, von Caemmerer S, Price GD, Badger MR and Fur-bank RT (1998) Expression of tobacco carbonic anhydrase in the C4 dicot Flaveria bidentis leads to increased leakiness of the bundle sheath and a defective CO2 -concentrating mecha-nism. Plant Physiol 117: 1071-1081PubMedGoogle Scholar
  67. Ludwig M, Sultemeyer D and Price GD (2000) Isolation of ccmKLMN genes from the marine cyanobacterium, Syne-chococcus sp PCC7002 (Cyanobacteria), and evidence that CcmM is essential for carboxysome assembly. J Phycol 36: 1109-1118Google Scholar
  68. Maeda S, Badger MR and Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobac-terium, Synechococcus sp PCC7942. Molec Microbiol 43: 425-435Google Scholar
  69. Majeau N, Arnoldo M and Coleman JR (1994) Modification of carbonic anhydrase activity by antisense and over-expression constructs in transgenic tobacco. Plant Mol Biol 25: 377-385PubMedGoogle Scholar
  70. McKay RML and Gibbs SP (1991) Composition and func-tion of pyrenoids: cytochemical and immunocytochemical ap-proaches. Can J Bot 69: 1040-1052Google Scholar
  71. McKay RML, Gibbs SP and Espie GS (1993) Effect of dissolved inorganic carbon on the expression of carboxysomes, localiza-tion of Rubisco and the mode of inorganic carbon transport in cells in the cyanobacterium Synechococcus UTEX 625. Arch Microbiol 159: 21-29Google Scholar
  72. Meldrum NU and Roughton FJW (1933) Carbonic anhydrase. Its preparation and properties. J Physiol 80: 113-142PubMedGoogle Scholar
  73. Mitra M, Lato SM, Ynalvez RA, Xiao Y and Moroney JV (2004) Identification of a chloroplast carbonic anhydrase in Chlamy-domonas reinhardtii. Plant Physiol 135: 173-182PubMedGoogle Scholar
  74. Mitra M, Mason CB, Xiao Y, Ynalvez RA, Lato SM and Moroney JV (2005) The carbonic anhydrase gene families of Chlamy-domonas reinhardtii. Can J Bot 83: 780-795Google Scholar
  75. Mitsuhashi S and Miyachi S (1996) Amino acid sequence ho-mology between N- and C-terminal halves of a carbonic anhy-drase in Porphyridium purpureum, as deduced from the cloned cDNA. J Biol Chem 271: 28703-28709PubMedGoogle Scholar
  76. Mitsuhashi S, Mizushima T, Yamashita E, Yamamoto M, Kumasaka T, Moriyama H, Ueki T, Miyachi S and Tsukihara T (2000) X-ray structure of beta-carbonic anhydrase from the red alga,Porphyridium purpureum, reveals a novel catalytic site for CO2 hydration. J Biol Chem 275: 5521-5526PubMedGoogle Scholar
  77. Miyao M (2003) Molecular evolution and genetic engineering of C4 photosynthesis enzymes. J Exp Bot 54: 179-189PubMedGoogle Scholar
  78. Morita E, Kuroiwa H, Kuroiwa T and Nozaki H (1997) High localization of ribulose 1,5-bisphosphate carboxy-lase/oxygenase in the pyrenoids of Chlamydomonas rein-hardtii (Chlorophyta) as revealed by cryofixation and immuno-gold electron microscopy. J Phycol 33: 68-72Google Scholar
  79. Morita E, Abe T, Tsuzuki M, Fujiwara S, Sato N, Hirata A, Sonoike K and Nozaki H (1998) Presence of the CO2 -concentrating mechanism in some species of the pyrenoid-less free living algal genus Chloromonas (Volvocales, Chloro-phyta). Planta 204: 269-276PubMedGoogle Scholar
  80. Morita E, Abe T, Tsuzuki M, Fujiwara S, Sato N, Hirata A, Sonoike K and Nozaki H (1999) Role of pyrenoids in the CO2 concentrating mechanism: comparative morphology, physiol-ogy and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas. Planta 208: 365-372Google Scholar
  81. Moroney JV and Mason CB (1991) The role of the chloroplast in Ci uptake in Chlamydomonas reinhardtii. Can J Bot 69: 1017-1024Google Scholar
  82. Moroney JV and Somanchi A (1999) How do algae concentrate CO2 to increase the efficiency of photosynthetic carbon fixa-tion? Plant Physiol 119: 9-16PubMedGoogle Scholar
  83. Moroney JV, Husic HD and Tolbert NE (1985) Effect of car-bonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79: 177-183PubMedGoogle Scholar
  84. Moroney JV, Bartlett SG and Samuelsson G (2001) Carbonic anhydrases in plants and algae. Plant Cell Environ 24: 141-153Google Scholar
  85. Newman T, DeBruijn FJ, Green P, Keegstra K, Kende H, McIntosh L, Ohlrogge J, Raikhel N, Somerville S, Thomashow M, Retzel E and Somerville C (1994) Genes galore: a sum-mary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106: 1241-1255PubMedGoogle Scholar
  86. Niles EG, Condit RC, Caro P, Davidson K, Matusick L and Seto J (1986) Nucleotide sequence and genetic map of the 16-kb vaccinia virus HindIII D fragment. Virology 153: 96-112PubMedGoogle Scholar
  87. Okada M (1992) Recent studies on the composition and activ-ity of algal pyrenoids. In: Round FE and Chapman DJ (eds) Progress in Phycological Research, Vol 8, pp 117-138. Bio-press Ltd, BristolGoogle Scholar
  88. Omata T, Price GD, Badger MR, Okamura M, Gohta S and Ogawa T (1999) Identification of an ATP-binding cassette trans-porter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp strain PCC 7942. Proc Natl Acad Sci USA 96: 13571-13576PubMedGoogle Scholar
  89. Or ús MI, Rodríguez ML, Martínez F and Marco E (1995) Bio-genesis and ultrastructure of carboxysomes from wild-type and mutants of Synechococcus sp strain PCC-7942. Plant Physiol 107: 1159-1166PubMedGoogle Scholar
  90. Osterlind S (1950) Inorganic carbon sources of green algae. I: growth experiments with Scenedesmus quadricauda and Chlorella pyrenoidosa. Physiol Plant 3: 353-360Google Scholar
  91. Palmqvist K, Yu JW and Badger MR (1994) Carbonic anhydrase activity and inorganic carbon fluxes in low and high Cicells of Chlamydomonas reinhardtii and Scenedesmus obliquus. Phys-iol Plant 90: 537-547Google Scholar
  92. Palmqvist K, S ültemeyer D, Baldet P, Andrews TJ and Bad-ger MR (1995) Characterization of inorganic fluxes, carbonic anhydrase(s) and ribulose-1,5-bisphosphate carboxylase-oxygenase in the green unicellular alga Coccomyxa. Planta 197: 352-361Google Scholar
  93. Parisi G, Perales M, Fornasari MS, Colaneri A, Gonzalez-Schain N, Gomez-Casati D, Zimmermann S, Brennicke A, Araya A, Ferry JG, Echave J and Zabaleta E (2004) Gamma carbonic anhydrases in plant mitochondria. Plant Mol Biol 55: 193-207PubMedGoogle Scholar
  94. Pierce J, Carlson TJ and Williams JGK (1989) A cyanobacterial mutant requiring the expression of Ribulose bisphosphate car-boxylase from a photosynthetic anaerobe. Proc Natl Acad Sci USA 86: 5753-5757PubMedGoogle Scholar
  95. Pollock SV, Prout DL, Godfrey AC, Lemaire SD and Moroney JV (2004) The Chlamydomonas reinhardtii proteins Ccp1 and Ccp2 are required for long- term growth but are not necessary for efficient photosynthesis, in a low CO2 environment. Plant Mol Biol 56: 125-132PubMedGoogle Scholar
  96. Price GD and Badger MR (1989) Expression of human carbonic-anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2 -requiring phenotype-evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol 91: 505-513PubMedGoogle Scholar
  97. Price GD, Coleman JR and Badger MR (1992) Association of carbonic-anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100: 784-793PubMedGoogle Scholar
  98. Price GD, Howitt SM, Harrison K and Badger MR (1993) Anal-ysis of a genomic DNA region from the cyanobacterium Synechococcus sp strain PCC7942 involved in carboxysome assembly and function. J Bact 175: 2871-2879PubMedGoogle Scholar
  99. Price GD, von Caemmerer S, Evans JR, Yu JW, Lloyd J, Oja V, Kell P, Harrison K, Gallagher A and Badger MR (1994) Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation. Planta 193: 331-340Google Scholar
  100. Price GD, S ültemeyer D, Klughammer B, Ludwig M and Badger MR (1998) The functioning of the CO2 concentrating mecha-nism in several cyanobacterial strain: a review of general phys-iological characteristics, genes, proteins, and recent advances. Can J Bot 76: 973-1002Google Scholar
  101. Price GD, Maeda S-I, Omata T and Badger MR (2002) Modes of active inorganic carbon uptake in the cyanobacterium, Syne-chococcus sp PCC7942. Funct Plant Biol 29: 131-149Google Scholar
  102. Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101: 18228-18233PubMedGoogle Scholar
  103. Rademacher T, Hausler RE, Hirsch H-J, Zhang L, Lipka V and Weier D (2002) An engineered phosphoenolpyruvate carboxy-lase redirects carbon and nitrogen flow in transgenic potato plants. Plant J 32: 25-39PubMedGoogle Scholar
  104. Ramazanov Z, Mason CB, Geraghty AM, Spalding MH and Moroney JV (1993) The low CO2 -inducible 36 kDa protein is localized to the chloroplast envelope of Chlamydomonas reinhardtii. Plant Physiol 101:1195-1199PubMedGoogle Scholar
  105. Raven JA (1997) CO2 -concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant Cell Environ 20: 147-154Google Scholar
  106. Raven JA, Johnston AM, K übler JE, Korb R, McInroy SG, Han-dley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredrikson S and Dunton KH (2002) Mechanistic interpre-tation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29: 355-378Google Scholar
  107. Rawat M and Moroney JV (1991) Partial characterization of a new isoenzyme of carbonic-anhydrase isolated from Chlamy-domonas reinhardtii. J Biol Chem 266: 9719-9723PubMedGoogle Scholar
  108. Rawat M, Henk MC, Lavigne LL and Moroney JV (1996) Chlamydomonas reinhardtii mutants without ribulose-1,5-bisphosphate carboxylase-oxygenase lack a detectable pyrenoid. Planta 198: 263-270Google Scholar
  109. Reinfelder JR, Kraepiel AML and Morel FMM (2001) Unicel-lular C4 photosynthesis in a marine diatom. Nature 407: 996-999Google Scholar
  110. Reinhold L, Hosloff R and Kaplan A (1991) A model for in-organic carbon fluxes and photosynthesis in cyanobacterial carboxysomes. Can J Bot 69:984-988Google Scholar
  111. Reiskind JB and Bowes G (1991) The role of phos-phoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proc Natl Acad Sci USA 88: 2883-2887PubMedGoogle Scholar
  112. Rowlett RS, Chance MR, Wirt MD, Sidelinger DE, Royal JR, Woodroffe M, Wang YFA, Saha RP and Lam MG (1994) Kinetic and structural characterization of spinach carbonic-anhydrase. Biochemistry 33: 13967-13976PubMedGoogle Scholar
  113. Ronen-Tarazi M, Lieman-Hurwitz J, Gabay C, Or ús MI and Kaplan A (1995) The genomic region of rbcLS in Synechococ-cus PCC 7942 contains genes involved in the ability to grow under low CO2 concentration and in chlorophyll biosynthesis. Plant Physiol 108: 1461-1469PubMedGoogle Scholar
  114. Schwarz R, Reinhold L and Kaplan A (1995) Low activation state of 1,5-bisphosphate carboxylase/oxygenase activation in carboxysome defective Synechococcus mutants. Plant Physiol 108: 183-190PubMedGoogle Scholar
  115. Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A and Ogawa T (2001) Distinct constitutive and low-CO2 -induced CO2 uptake systems in cyanobacteria: novel genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98: 11789-11794PubMedGoogle Scholar
  116. Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A and Ogawa T (2002) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria. J Biol Chem 277: 18658-18664PubMedGoogle Scholar
  117. Silverman DN (2000) Marcus rate theory applied to enzymatic proton transfer. Biochem Biophys Acta Bioenerg 1458: 88-103Google Scholar
  118. Smith EC and Griffiths H (1996a) The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2 -concentrating mechanism and carbon isotope discrim-ination in lichens and bryophytes. Planta 198: 6-16Google Scholar
  119. Smith EC and Griffiths H (1996b) A pyrenoid based carbon con-centrating mechanism is present in terrestrial bryophytes of the class anthocerotae. Planta 200: 203-212Google Scholar
  120. Smith EC and Griffiths H (2000) The role of carbonic anhydrase in photosynthesis and the activity of the carbon concentrat-ing mechanism in bryophytes of the class Anthocerotae. New Phytol 145: 29-37Google Scholar
  121. Smith KS and Ferry JG (1999) A plant-type (beta-class) carbonic anhydrase in the thermophilic methanoarchaeon Methanobac-terium thermoautotrophicum. J Bact 181: 6247-6253PubMedGoogle Scholar
  122. So AKC and Espie GS (1998) Cloning, characterization and expression of carbonic anhydrase from the cyanobacterium Synechocystis PCC 6803. Plant Mol Biol 37: 205-215PubMedGoogle Scholar
  123. So AKC, Cot SSW and Espie GS (2002) Characterization of the C-terminal extension of carboxysomal carbonic anhydrase from Synechocystis sp. PCC6803. Funct Plant Biol 29: 183-194Google Scholar
  124. So AKC, Espie GS, Williams EB, Shively JM, Heinhorst S and Cannon GC (2004) A novel evolutionary lineage of carbonic anhydrase (ε class) is a component of the carboxysome shell. J Bacteriol 186: 623-630PubMedGoogle Scholar
  125. Soltes-Rak E, Mulligan ME and Coleman JR (1997) Identifica-tion and characterization of a gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria. J Bact 179: 769-774PubMedGoogle Scholar
  126. Spalding MH and Ogren WL (1982) Photosynthesis is required for induction of the CO2 -concentrating system in Chlamy-domonas reinhardtii. FEBS Lett 145: 41-44Google Scholar
  127. Starr RC and Zeikus JA (1993) UTEX- the culture collection of algae at the University of Texas at Austin. J Phycol 29: 1-106Google Scholar
  128. Strayer DS and Jerng HH (1992) Sequence and analysis of the BamH1 “D” fragment of Shope fibroma virus: comparison with similar regions of related poxviruses. Virus Res 25: 117-132PubMedGoogle Scholar
  129. S ültemeyer DF, Price GD, Yu JW and Badger MR (1995) Char-acterization of carbondioxide and bicarbonate transport dur-ing steady state photosynthesis in the marine cyanobacterium Synechococcus strain PCC 7002. Planta 197: 597-607Google Scholar
  130. Takano J, Noguchi K, Yasumor M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T and Fujiwara T (2002) Arabidopsis boron transporter for xylem loading. Nature 420: 337-340PubMedGoogle Scholar
  131. Thielmann J, Tolbert NE, Goyal A and Senger H (1989) Two systems for CO2 and bicarbonate during photosynthesis by Scenedesmus. Plant Physiol 92: 622-629Google Scholar
  132. Tripp B, Bell C, Cruz F, Krebs C and Ferry JG (2004) A role for iron in an ancient carbonic anhydrase. J Biol Chem 279: 6683-6687PubMedGoogle Scholar
  133. Tsuzuki M and Miyachi S (1989) The function of carbonic anhydrase in aquatic photosynthesis. Aqua Bot 34: 85-104Google Scholar
  134. Tsuzuki M and Miyachi S (1991) CO2 syndrome in Chlorella. Can J Bot 69: 1003-1007Google Scholar
  135. Turpin DH, Miller AG and Canvin DT (1984) Carboxysome con-tent of Synechococcus leopoliensis (Cyanophyta) in response to inorganic carbon. J Phycol 20: 249-253Google Scholar
  136. Tyerman SD, Niemietz CM and Bramley H (2002) Plant aquapor-ins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25: 173-194PubMedGoogle Scholar
  137. Van Hunnik E, Livine A, Pogenberg V, Spijkerman E, van den Ende H, Mendoza EG, S ültemeyer D and de Leeuw JW (2001) Identification and localization of a thylakoid bound carbonic anhydrase from the green alga Tetraedron minimum (Chloro-phyta) and Chlamydomonas noctigama (Chlorophyta). Planta 212: 454-459PubMedGoogle Scholar
  138. Vidal J and Chollet R (1997) Regulation of C4 PEP carboxylase. Trends Plant Sci 2: 230-237Google Scholar
  139. Voznesenskaya EV, Franceschi VR, Kiirats O, Artyusheva EG, Freitag H and Edwards GE (2002) Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodi-aceae) Plant J 31: 649-662PubMedGoogle Scholar
  140. Whitney SM, Baldet P, Hudson GS and Andrews TJ (2001) Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Plant J 26: 535-547PubMedGoogle Scholar
  141. Yang Z, Zhang Q and Xu Z (1999) Cloning of a cDNA of a du-plicated carbonic anhydrase in Dunaliella salina. (Accession number AAF22644)Google Scholar
  142. Yu JW, Price GD, Song L and Badger MR (1992) Isolation of a putative carboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100:794-800PubMedGoogle Scholar
  143. Yu JW, Price GD and Badger MR (1994) Characterization of CO2 and HCO3 uptake during steady state photosynthesis in the cyanobacterium Synechococcus PCC 7942. Aust J Plant Physiol 21: 185-195Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Sue G. Bartlett
    • 1
  • Mautusi Mitra
    • 1
  • James V. Moroney
    • 1
  1. 1.Biochemistry and Molecular Biology Section, Department of Biological SciencesLouisiana State UniversityBaton RougeUSA

Personalised recommendations