Physiological and Molecular Studies on the Response of Cyanobacteria to Changes in the Ambient Inorganic Carbon Concentration

  • Aaron Kaplan
  • Rakefet Schwarz
  • Judy Lieman-Hurwitz
  • Michal Ronen-Tarazi
  • Leonora Reinhold
Part of the Advances in Photosynthesis book series (AIPH, volume 1)


The ability of cyanobacteria to adapt to a wide range of ambient CO2 concentrations involves modulation of the activity of an inorganic carbon-concentrating mechanism (CCM), as well as other changes at various cellular levels including the biosynthetic pathway of purines. Studies of high-CO2-requiring mutants have identified several of the genes involved in the operation of the CCM and in the ability to grow under changing ambient CO2 concentration. In the case of Synechococcus sp. strain PCC 7942 most of these genes have been mapped in the genomic region of the rbcLS operon. Higher levels of detectable transcripts originating from some of these genes have been observed after exposure of the cells to low CO2 concentration. Studies of mutants have confirmed quantitative models postulating crucial roles for carboxysomes and carboxysome-located carbonic anhydrase (CA) in cyanobacterial photosynthesis. A central role is also proposed for cytoplasmic-membrane-associated CA activity: CA may function to scavenge escaping CO2 by intracellular conversion to bicarbonate against the chemical potential.


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  1. Aizawa K and Miyachi S (1986) Carbonic anhydrase and CO2 concentrating mechanism in microalgae and cyanobacteria. FEMS Microbiol Rev 39: 215–233.CrossRefGoogle Scholar
  2. Badger MR (1987) The CO2-concentrating mechanism in aquatic phototrophs. In: The Biochemistry of Plants, Vol 10, pp 219–274. Academic Press, New York.Google Scholar
  3. Badger MR and Price GD (1992) The CO2 concentrating mechanism of cyanobacteria and green algae. Physiol Plant 84: 606–615.CrossRefGoogle Scholar
  4. Badger MR, Basset M and Comins HM (1985) A model for HCO3 - accumulation and photosynthesis in the cyanobacterium Synechococcus sp. Plant Physiol 77: 465–471.PubMedCrossRefGoogle Scholar
  5. Bedu S, Beuf L and Joset F (1992) Membranous and soluble carbonic anhydrase activities in a cyanobacterium, Synecho-cystis PCC6803. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 819–822. Kluwer, Dordrecht.CrossRefGoogle Scholar
  6. Berry JA (1989) Studies of mechanisms affecting the fractionation of carbon isotopes in photosynthesis. In: Rundel PW, Ehleringer JR and Nagy KA (eds) Stable Isotopes in Ecological Research, pp 82–94. Springer-Verlag, New York.CrossRefGoogle Scholar
  7. Bloye SA, Silman NJ, Mann NH and Carr NG (1992) Bicarbonate concentration by Synechocystis PCC6803. Plant Physiol 99: 601–606.PubMedCrossRefGoogle Scholar
  8. Brown II, Fadeyev SI, Kirik II, Severina II and Skulachev VP (1990) Light-dependent delta μNa-generation and utilization in the marine cyanobacterium Oscillatoria brevis. FEBS Lett 270: 203–206.PubMedCrossRefGoogle Scholar
  9. Coleman JR (1991) The molecular and biochemical analyses of CO2-concentrating mechanisms of cyanobacteria and green algae. Plant Cell Environ 14: 861–867.CrossRefGoogle Scholar
  10. Codd GA (1988) Carboxysomes and ribulose bisphosphate carboxylase/oxygenase. In: Ross AH and Tempest DW (eds) Advances in Microbial Physiology, Vol 29, pp 115–164. Academic Press, London.Google Scholar
  11. Eaton-Rye J, Blubaugh DJ and Govindjee (1986) Action of bicarbonate on photosynthetic electron transport in the presence or absence of inhibitory anions. In: Barber J, Papa S and Papageorgiou G (eds) Ion Interactions in Energy Transport Systems, pp 263–278. Plenum Press, New York.CrossRefGoogle Scholar
  12. Ebbole D and Zalkin H (1987) Cloning and characterization of a 12-gene cluster from Bacillus subtilis encoding nine enzymes for de novo purine nucleotide synthesis. J Biol Chem 262: 8274–8287.PubMedGoogle Scholar
  13. Espie GS and Kandasamy RA (1992) Na+-independent HCO3 -transport and accumulation in the cyanobacterium Synechococcus UTEX 625. Plant Physiol 98: 560–568.PubMedCrossRefGoogle Scholar
  14. Friedberg D, Kaplan A, Ariel R, Kessel M and Seijffers J (1989) The 5’ flanking region of the gene encoding the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is crucial for growth of the cyanobacterium Synechococcus PCC7942 in air level of CO2. J Bacteriol 171: 6069–6076.PubMedGoogle Scholar
  15. Fukuzawa H, Suzuki E, Komukai Y and Miyachi S (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon fixation in the cyanobacterium Synechococcus PCC7942. Proc Natl Acad Sci USA 89: 4437–4441.PubMedCrossRefGoogle Scholar
  16. Hassidim M, Schwarz R, Lieman-Hurwitz J, Marco E, Ronen-Tarazi M and Kaplan A (1992) A cyanobacterial gene encoding peptidyl-prolyl cis-trans isomerase. Plant Physiol 100: 1982–1986.PubMedCrossRefGoogle Scholar
  17. Holthijzen YA, van Breemen JFL, Kuenen JG and Konings L (1986) Protein composition of the carboxysomes of Thiobacillus neopolitanus. Arch Microbiol 144: 398–404.CrossRefGoogle Scholar
  18. Jager KM and Bergman B (1991) Localization of a multifunctional chaperonin (GroEL protein) in nitrogen-fixing Anabaena PCC 7120: presence in vegetative cells and heterocysts. Planta 183: 120–125.CrossRefGoogle Scholar
  19. Kaplan A, Badger MR and Berry JA (1980) Photosynthesis and intracellular inorganic carbon pool in the blue-green algae Anabaena variabilis: response to external CO2 concentration. Planta 149: 219–226.CrossRefGoogle Scholar
  20. Kaplan A, Zenvirth D, Marcus Y, Omata T and Ogawa T (1987) Energization and activation of inorganic carbon uptake by light in cyanobacteria. Plant Physiol 84: 210–213.PubMedCrossRefGoogle Scholar
  21. Kaplan A, Scherer S and Lerner M (1989) Nature of the light-induced H+ efflux and Na+ uptake in cyanobacteria. Plant Physiol 89: 1220–1225.PubMedCrossRefGoogle Scholar
  22. Kaplan A, Schwarz R, Ariel R and Reinhold L (1990) The ‘CO2 concentrating mechanism’ of cyanobacteria: physiological molecular and theoretical studies. In: Kanai R, Katoh S and Miyachi S (eds) Regulation of Photosynthetic Processes. Bot Mag (special issue) 2: 53–72.Google Scholar
  23. 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.PubMedCrossRefGoogle Scholar
  24. Lanaras T, Hawthornthwaite AM and Codd GA (1985) Localization of carbonic anhydrase in the cyanobacterium Chlorogloeopsis fritschii. FEMS Microbiol Lett 26: 285–288.CrossRefGoogle Scholar
  25. Lieman-Hurwitz J, Schwarz R, Martinez F, Maor Z, Reinhold L and Kaplan A (1990) Molecular analysis of high-CO2 requiring mutants indicates that genes in the region of rbc are involved in the ability of cyanobacteria to grow under low CO2. Can J Bot 69: 945–950.CrossRefGoogle Scholar
  26. Marco M, Ohad N, Schwarz R, Lieman-Hurwitz J, Gabay C and Kaplan A (1993) High CO2 concentration alleviates the block in photosynthetic electron transport in an ndhB-inactivated mutant of Synechococcus sp. PCC 7942. Plant Physiol 101: 1047–1053.PubMedCrossRefGoogle Scholar
  27. Marcus Y, Zenvirth D, Harel E and Kaplan A (1982) Induction of HCO3 - transporting capability and high photosynthetic affinity to inorganic carbon by low concentration of CO2 in Anabaena variabilis. Plant Physiol 69: 1008–1012.PubMedCrossRefGoogle Scholar
  28. Marcus Y, Schwarz R, Friedberg D and Kaplan A (1986) High CO2 requiring mutant of Anacystis nidulans R2. Plant Physiol 82: 610–612.PubMedCrossRefGoogle Scholar
  29. Marcus Y, Berry JA and Pierce J (1992) Photosynthesis and photorespiration in a mutant of the cyanobacterium Synechocystis PCC6803 lacking carboxysomes. Planta 187: 511–516.CrossRefGoogle Scholar
  30. Marek LF and Spalding MH (1991) Changes in photorespiratory enzyme activity in response to limiting CO2 in Chlamydomonas reinhardtii. Plant Physiol 97: 420–425.PubMedCrossRefGoogle Scholar
  31. Mayo MP, Elrifi IR and Turpin DH (1989) The relationship between ribulose bisphosphate concentration, dissolved inorganic carbon (DIC) transport and DIC-limited photosynthesis in the cyanobacterium Synechococcus leopoliensis grown at different concentrations of inorganic carbon. Plant Physiol 90: 720–727.PubMedCrossRefGoogle Scholar
  32. McKay RML, Gibbs SP and Espie GS (1992) Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of RubisCO and the mode of inorganic carbon transport in cells of the cyanobacterium Synechococcus UTEX 625. Arch Microbiol 159: 21–29.CrossRefGoogle Scholar
  33. Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1992) Electron donation from cyclic and respiratory flow to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33: 1233–1238.Google Scholar
  34. Miller AG and Canvin DR (1985) Distinction between HCO3 -and CO2-dependent photosynthesis in the cyanobacterium Synechococcus leopoliensis based on the selective response of HCO3 - transport to Na+. FEBS Lett 187: 29–32.CrossRefGoogle Scholar
  35. Miller AG, Espie GS and Canvin DT (1988) Chlorophyll a fluorescence yield as a monitor of both active CO2 and HCO3 -transport by the cyanobacterium Synechococcus UTEX 625. Plant Physiol 86: 655–658.PubMedCrossRefGoogle Scholar
  36. Miller AG, Espie GS and Canvin DT (1990) Physiological aspects of CO2 and HCO3 - transport by cyanobacteria: a review. Can J Bot 68: 1291–1302.CrossRefGoogle Scholar
  37. Myers J (1992) Responses of Synechococcus 6301 to low DIC. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 791–794. Kluwer, Dordrecht.CrossRefGoogle Scholar
  38. Nicholls P, Obinger C, Niederhauser H and Pcschck GA (1992) Cytochrome oxidase in Anacystis nidulans: stoichiometrics and possible functions in the cytoplasmic and thylakoid membranes. Biochim Biophys Acta 1098: 184–190.CrossRefGoogle Scholar
  39. Ogawa T (1991) A gene homologous to the subunit-2 gene of N ADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC 6803. Proc Natl Acad Sci USA 88: 4275–4279.PubMedCrossRefGoogle Scholar
  40. Ogawa T (1992) Identification and characterization of the ictA/ ndhL gene product essential to inorganic carbon transport of Synechocystis PCC 6803. Plant Physiol 99: 1604–1608.PubMedCrossRefGoogle Scholar
  41. Ogawa T (1993) Molecular analysis of the CO2-conccntrating mechanism in cyanobacteria. In: Yamamoto H and Smith C (eds) Photosynthetic Responses to the Environment, pp 113–125. American Society of Plant Physiology, Rockville, MDGoogle Scholar
  42. Ogawa T and Kaplan A (1987) The stoichiometry between CO2 and H+ fluxes involved in the transport of inorganic carbon in cyanobacteria. Plant Physiol 83: 888–891.PubMedCrossRefGoogle Scholar
  43. Ogawa T, Miyano A and Inoue Y (1985) Photosystem-I-driven inorganic carbon transport in the cyanobacterium, Anacystis nidulans. Biochim Biophys Acta 808: 77–84.CrossRefGoogle Scholar
  44. Ogawa T, Kaneda T and Omata T (1987) A mutant of Synechococcus PCC 7942 incapable of adapting to low CO2 concentration. Plant Physiol 84: 711–715.PubMedCrossRefGoogle Scholar
  45. Ogura Y, Takemura M, Oda K, Yamato K, Ohta H, Fukuzawa H and Ohyama K (1992) Cloning and nucleotide sequence of a frxC-ORF469 gene cluster of Synechocystis PCC6803: conservation with liverwort chloroplast frxC-ORF465 and nif Operon. Biosci Biotechnol Biochem 56: 788–793.PubMedCrossRefGoogle Scholar
  46. Omata T (1992) Characterization of the downstream region of cmpA: identification of a gene cluster encoding a putative permease of the cyanobacterium Synechococcus PCC7942. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 807–810. Kluwer, Dordrecht.CrossRefGoogle Scholar
  47. Omata T and Ogawa T (1986) Biosynthesis of a 42KD polypeptide in the cytoplasmic membrane of the cyanobacterium Anacystis nidulans strain R2 during adaptation to low concentration. Plant Physiol 80: 525–530.PubMedCrossRefGoogle Scholar
  48. Omata T, Carlson TJ, Ogawa T and Pierce J (1990) Sequencing and modification of the gene encoding the 42-kilodalton protein in the cytoplasmic membrane of Synechococcus PCC 7942. Plant Physiol 93: 305–311.PubMedCrossRefGoogle Scholar
  49. Orus MI, Martinez F, Rodriguez ML and Marco E (1992) Ultrastructural study of carboxysomes from high-CO2 requiring mutants of Synechococcus PCC 7942. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 787–790. Kluwer, Dordrecht.CrossRefGoogle Scholar
  50. Peschek GA (1987) Respiratory and electron transport. In: Fay P and Van Baalen C (eds) The Cyanobacteria, pp 119–161. Elsevier Science Publishers, Amsterdam.Google Scholar
  51. Pierce J and Omata T (1988) Uptake and utilization of inorganic carbon by cyanobacteria. Photosynth Res 16: 141–154.CrossRefGoogle Scholar
  52. Pierce J, Carlson TJ and Williams JGK (1988) Anomalous oxygen sensitivity in a cyanobacterial mutant requiring the expression of ribulosebisphosphate carboxylase from a photosynthetic anaerobe. Proc Nat Acad Sci USA 86: 5753–5757.CrossRefGoogle Scholar
  53. Price GD and Badger MR (1989a) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC 7942 creates a high CO2 requiring phenotype. Plant Physiol 91: 505–513.PubMedCrossRefGoogle Scholar
  54. Price GD and Badger MR (1989b) Isolation and characterization of high-CO2 requiring mutants of the cyanobacterium Synechococcus PCC7942. Two phenotypes that accumulate inorganic carbon but are apparently unable to generate CO2 within the carboxysomes. Plant Physiol 91: 514–525.PubMedCrossRefGoogle Scholar
  55. Price GD and Badger MR (1991) Evidence for the role of carboxysomes on cyanobacterial CO2-concentrating mechanism. Can J Bot 69: 963–973.CrossRefGoogle Scholar
  56. Price GD, Coleman JR and Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100: 784–793.PubMedCrossRefGoogle Scholar
  57. Price GD, Howitt SM, Harrison K and Badger MR (1993) Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. J Bacteriol 175: 2871–2879.PubMedGoogle Scholar
  58. Raven JA (1991) implications of inorganic C utilization: Ecology, evolution and geochemistry. Can J Bot 69: 908–924.CrossRefGoogle Scholar
  59. Reddy KJ, Masamoto K, Sherman DM and Sherman LA (1989) DNA sequence and regulation of the gene (cpbA) encoding the 42-kilodalton cytoplasmic membrane carotenoprotein of the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 171: 3486–3493.PubMedGoogle Scholar
  60. Reinhold L, Volokita M, Zenvirth D and Kaplan A (1984) Is HCO3 - transport in Anabaena a Na+-symport?. Plant Physiol 76: 190–192.CrossRefGoogle Scholar
  61. Reinhold L, Zviman M and Kaplan A (1989). A quantitative model for inorganic carbon fluxes and photosynthesis in cyanobacteria. Plant Physiol and Biochem 27: 945–954.Google Scholar
  62. Reinhold L, Kosloff R and Kaplan A (1991) A model for inorganic carbon fluxes and photosynthesis in cyanobacterial carboxysomes. Can J Bot 69: 984–988.CrossRefGoogle Scholar
  63. Scanlan DJ, Bloye SA, Mann NH, Hodgson DA and Carr NG (1990) Construction of lacZ promoter probe vectors for use in Synechococcus: application to the identification of CO2-regulated promoters. Gene 90: 43–49.PubMedCrossRefGoogle Scholar
  64. Schluchter WM, Zhao J and Bryant DA (1993) Isolation and characterization of the ndhF gene of Synechococcus sp. strain PCC 7002 and initial characterization of an interposon mutant. J Bacteriol 175: 3343–3352.PubMedGoogle Scholar
  65. Schwarz R, Friedberg D, Reinhold L and Kaplan A (1988) Is there a role for the 42kDa polypeptide in inorganic carbon uptake by cyanobacteria?. Plant Physiol 88: 284–288.PubMedCrossRefGoogle Scholar
  66. Schwarz R, Lieman-Hurwitz J, Hassidim M and Kaplan A (1992a) Phenotypic complementation of high-CO2-requiring mutants of the cyanobacterium Synechococcus sp. strain PCC 7942 by inosine 5′-monophosphate. Plant Physiol 100: 1987–1993.PubMedCrossRefGoogle Scholar
  67. Schwarz R, Lieman-Hurwitz J, Marco E, Ronen-Tarazi M, Ohad N, Hassidim M, Gabay C, Reinhold L and Kaplan A (1992b) The CO2-concentrating mechanism of cyanobacteria: elucidation with the aid of high-CO2-requiring mutants. In: Murata N (ed) Research in Photosynthesis, Vol III, pp 437–440. Kluwer, Dordrecht.CrossRefGoogle Scholar
  68. Spalding MH and Ogren WL (1982) Photosynthesis is required for induction of the CO2-concentrating system in Chlamy-domonas reinhardtii. FEBS Lett 145: 41–44.CrossRefGoogle Scholar
  69. Suzuki E, Fukuzawa H, Abe T and Miyachi S (1991) Identification of the genomic region which complements a temperature-sensitive, high CO2 requiring mutant of the cyanobacterium Synechococcus PCC7942. Mol Gen Genet 226: 401–408.PubMedCrossRefGoogle Scholar
  70. Tu CK, Spiller H, Wynns GC and Silverman DN (1987) Carbonic anhydrase and the uptake of inorganic carbon by Synechococcus sp. (UTEX 2380). Plant Physiol 85: 72–77.PubMedCrossRefGoogle Scholar
  71. Turpin DH, Miller AG and Canvin DT (1984) Carboxysome content of Synechococcus leopoliensis (Cyanophyta) in response to inorganic carbon. J Phycol 20, 249–253.CrossRefGoogle Scholar
  72. Volokita M, Zenvirth D, Kaplan A and Reinhold L (1984) Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol 76: 599–602.PubMedCrossRefGoogle Scholar
  73. Yu L, Golbeck JH, Zhao J, Schluchter WM, Muehlenhoff U and Bryant D (1992) The PsaE protein is required for cyclic electron flow around photosystem I in the cyanobacterium Synechococcus PCC 7002. In: Murata N (ed) Research in Photosynthesis, Vol I, pp 565–568. Kluwer, Dordrecht.Google Scholar
  74. Yu L, Zhao J, Mühlenhoff U, Bryant DA, and Golbeck JH (1993) PsaE is required for in vivo cyclic electron flow around photosystem I in the cyanobacterium Synechococcus sp. PCC 7002. Plant Physiol 103: 171–180.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1994

Authors and Affiliations

  • Aaron Kaplan
    • 1
  • Rakefet Schwarz
    • 1
  • Judy Lieman-Hurwitz
    • 1
  • Michal Ronen-Tarazi
    • 1
  • Leonora Reinhold
    • 1
  1. 1.Department of BotanyThe Hebrew University of JerusalemJerusalemIsrael

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