Photosynthesis Research

, Volume 58, Issue 1, pp 25–42

Diurnal rhythms in metabolism: A day in the life of a unicellular, diazotrophic cyanobacterium

  • Louis A. Sherman
  • Pascal Meunier
  • Milagros S. Colón-López
Article

Abstract

N2 fixation and oxygenic photosynthesis are important metabolic processes that are at odds with each other, since the N2-fixing enzyme, nitrogenase, is highly sensitive to oxygen. This review will discuss the strategies devised by the unicellular, diazotrophic cyanobacterium, Cyanothece sp. ATCC 51142, to permit N2 fixation and photosynthesis to coexist in the same cell. This strain, like a number of other unicellular and filamentous (non-heterocystous) cyanobacteria, has developed a type of temporal regulation in which N2 fixation and photosynthesis occur at different times throughout a diurnal cycle. For nitrogenase, everyday dawns anew. The nifHDK operon is tightly regulated, such that transcription and translation occur within the first four hours of the dark period; nitrogenase is then proteolytically degraded. Photosynthesis also varies throughout the day reaching a minimum at the peak of nitrogenase activity and a maximum by late afternoon. This review will mainly concentrate on the various changes that occur in the photosynthetic apparatus as the cell modulates O2 evolution. The results indicate that the redox poise of the plastoquinone pool and the overall cellular energy needs are the basic driving forces behind these changes in the photosynthetic apparatus. Throughout the course of the diurnal cycle, Photosystem II becomes very heterogeneous as determined by 77 K fluorescence spectra, PAM fluorescence and O2-flash yield experiments. This system provides some important insight into cyanobacterial state transitions and, especially, on the organization of the photosystems within the membrane. Overall, PS II is altered on both the oxidizing and reducing sides of the photosystem.

circadian rhythms fluorescence gene regulation N2 fixation photosynthesis state transitions 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen MM(1988) Inclusions: Cyanophycin. Methods Enzymol 167: 207–213Google Scholar
  2. Allen MM and Weathers, PJ (1980) Structure and composition of cyanophycin granules in the cyanobacterium Aphanocapsa 6308. J Bacteriol 141: 959–962Google Scholar
  3. Apte SK (1996) Inter-relationship between photosynthesis and nitrogen fixation in cyanobacteria. J Sci Indust Res 55: 583–595Google Scholar
  4. Bader KP, Thibault P and Schmid GH (1983) A study on oxygen evolution and on the S-state distribution in thylakoid preparations of the filamentous blue-green alga Oscillatoria chalybea. Z Naturforsch 38c: 778–792Google Scholar
  5. Bald D, Kruip J and Rögner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: How is the phycobilisome connected with the photosystems? Photosynth Res 49: 103–118Google Scholar
  6. Bendall DS and Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229: 23–38Google Scholar
  7. Bergman B, Gallon JR, Rai AN and Stal LJ (1997) N2-fixation by non-heterocystous cyanobacteria. FEMSMicrobiol Rev 19: 139– 185Google Scholar
  8. Boichenko VA, Klimov VV, Mayes SR and Barber J (1993) Characterization of the light-induced oxygen gas exchange from the IC2 deletion mutant of Synechocystis PCC 6803 lacking the Photosystem II 33 kDa extrinsic protein. Z Naturforsch 48c: 224–233Google Scholar
  9. Bruce D, Brimble S and Bryant DA (1989) State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974: 66–73Google Scholar
  10. Buikema WJ and Haselkorn R (1993) Molecular genetics of cyanobacterial development. Annu Rev Plant Physiol Plant Mol Biol 44: 33–52Google Scholar
  11. Burnap RL and Sherman LA (1991) Deletion mutagenesis in Synechocystis sp. PCC 6803 indicates that the Mn-stablizing protein of Photosystem II is not essential for O2-evolution. Biochemistry 30: 440–446Google Scholar
  12. Burnap RL, Shen JR, Jursinic PA, Inoue Y and Sherman LA (1992) Oxygen yield and thermoluminescence characteristics of a cyanobacterium lacking the manganese-stabilizing protein of Photosystem II. Biochemistry 31: 7404–7410Google Scholar
  13. Burnap RL, Qian M and Pierce C (1996) The manganese-stabilizing protein of Photosystem II modifies the in vivo deactivation and photoactivation kinetics of the H2O oxidation complex in Synechocystis sp. PCC 6803. Biochemistry 35: 874–882Google Scholar
  14. Bustos SA and Golden SS (1992) Light-regulated expression of the psbD gene family in Synechococcus sp. strain PCC 7942: Evidence for the role of duplicated psbD genes in cyanobacteria. Mol Gen Genet 232: 221–230Google Scholar
  15. Campbell D and Öquist G (1996) Predicting light acclimation in cyanobacteria from nonphotochemical quenching of Photosystem II fluorescence, which reflects state transitions in these organisms. Plant Physiol 111: 1293–1298Google Scholar
  16. Campbell D, Bruce D, Carpenter C, Gustafsson P and Öquist G (1996) Two forms of the Photosystem II D1 protein alter energy dissipation and state transitions in the cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 47: 131–144Google Scholar
  17. Chen TH, Pen SY and Huang TC (1993) Induction of nitrogen-fixing circadian-rhythm Synechococcus RF-1 by light signals. Plant Sci 92: 179–182Google Scholar
  18. Cheniae GM and Martin IF (1972) Effects of hydroxylamine on Photosystem II. II. Photoreversal of the NH2OH destruction of O2 evolution. Plant Physiol 50: 87–94Google Scholar
  19. Chou HM and Huang TC (1991) Ultrastructure of the aerobic, nitrogen-fixing unicellular cyanobacterium Synechococcus sp. RF-1. In: Kausch H, Lampert W and Lhotsky O (eds) Archiv für Hydrobiologie, Algological Studies 64, pp 53–59. E. Schweizerbart’sche Verlagsbuchhandlung, StuttgartGoogle Scholar
  20. Colón-López MS, Sherman DM and Sherman LA (1997) Transcriptional and translational regulation of nitrogenase in lightdark and continuous-light grown cultures of the unicellular cyanobacterium, Cyanothece sp. ATCC 51142. J Bacteriol 179: 4319–4327Google Scholar
  21. Colón-López MS and Sherman LA (1998) Transcriptional and translational regulation of Photosystem I and II genes in lightdark and continuous-light-grown cultures of the unicellular cyanobacterium, Cyanothece sp. ATCC 51142. J Bacteriol 180: 519–526Google Scholar
  22. Dean DR and Jacobson MR (1992) Biochemical genetics of nitrogenase. In: Stacey G, Burris RH and Evans HJ (eds) Biological Nitrogen Fixation, pp 763–834. Chapman and Hall, New YorkGoogle Scholar
  23. Diner BA (1977) Dependence of the deactivation reactions of Photosystem II on the redox state of plastoquinone pool varied under anaerobic conditions. Equilibria on the acceptor side of Photosystem II. Biochim Biophys Acta 460: 247–258Google Scholar
  24. Engels DH, Lott A, Schmid GH and Pistorious EK (1994) Inactivation of the water-oxidizing enzyme in manganese stabilizing protein-free mutant cells of the cyanobacteria Synechococcus PCC 7942 and Synechocystis PCC 6803 during the dark incubation and conditions leading to photoactivation. Photosynth Res 42: 227–244Google Scholar
  25. Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56: 340–373Google Scholar
  26. Gallon JR (1981) The oxygen sensitivity of nitrogenase: A problem for biochemists and microorganisms. TIBS 6: 9–23Google Scholar
  27. Gallon JR (1992) Tansley Review No. 44. Reconciling the incompatible: N2 fixation and O2. New Phytol 122: 571–609Google Scholar
  28. Gallon JR and Chaplin AE (1987) An Introduction to Nitrogen Fixation. Cassell, London, UKGoogle Scholar
  29. Gleiter HM, Haag E, Shen JR, Eaton-Rye JJ, Seeliger AG, Inoue Y, Vermaas WFJ and Renger G (1995) Functional characterization of mutant strains of the cyanobacterium Synechocystis sp. PCC 6803 lacking short domains within the large, lumenexposed loop of the chlorophyll protein CP-47 in Photosystem II. Biochemistry 34: 6847–6856Google Scholar
  30. Golden SS, Brusslan J and Haselkorn R (1986) Expression of a family of psbA genes encoding a Photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5: 2789–2798Google Scholar
  31. Golden SS, Ishiura M, Johnson CH and Kondo T (1997) Cyanobacterial circadian rhythms. Annu Rev Plant Physiol Plant Mol Biol 48: 327–354Google Scholar
  32. Grobbelaar N, Huang TC, Lin HY and Chow TJ (1986) Dinitrogen fixing endogenous rhythm in Synechococcus RF1. FEMS Microbiol Lett 37: 173–177Google Scholar
  33. Grobbelaar N, Lin HY and Huang TC (1987) Induction of a nitrogenase activity rhythm in Synechococcus and the protection of its nitrogenase against photosynthetic oxygen. Curr Microbiol 15: 29–33Google Scholar
  34. Haselkorn R (1978) Heterocysts. Annu Rev Plant Physiol 29: 319– 344Google Scholar
  35. Haselkorn R (1986) Organization of the genes for nitrogen fixation in photosynthetic bacteria and cyanobacteria. Annu Rev Microbiol 40: 525–547Google Scholar
  36. Haselkorn R (1992) Developmentally regulated gene rearrangements in prokaryotes. Annu Rev Genet 26: 113–130Google Scholar
  37. Haselkorn R and Buikema WJ (1992) Nitrogen fixation in cyanobacteria. In: Stacey G, Burris RH and Evans HJ (eds) Biological Nitrogen Fixation, pp166–190. Chapman and Hall, New YorkGoogle Scholar
  38. Hirano M, Satoh K and Katoh S (1980) Plastoquinone as a common link between photosynthesis and respiration in blue-green alga. Photosynth Res 1: 149–162Google Scholar
  39. Howard JB and Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96: 2965–2982Google Scholar
  40. Huang TC and Chow TJ (1986) New type of N2-fixing unicellular cyanobacterium (blue-green alga). FEMS Microbiol Lett 36: 109–110Google Scholar
  41. Huang TC and Chou WM (1991) Setting the circadian rhythm of the prokaryotic Synechococcus sp. RF1 while its nif gene is repressed. Plant Physiol 96: 324–326Google Scholar
  42. Huang TC, Chow TJ and Hwang IS (1988) The cyclic synthesis of the nitrogenase of Synechococcus RF1 and its control at the transcriptional level. FEMS Microbiol Lett 50: 127–130Google Scholar
  43. Huang TC, Tu J, Chow TJ and Chen TH (1990) Circadian rhythm of the prokaryote Synechococcus sp. RF1. Plant Physiol 92: 531– 533Google Scholar
  44. Huang TC, Lay KC and Tong SR (1991) Resetting the endogenous circadian N-2-fixing rhythm of the prokaryote Synechococcus RF-1. Bot Bull Acad Sin 32: 129–133Google Scholar
  45. Huang T-C, Wang S-T and Grobbelaar N (1993) Circadian rhythm mutants of the prokaryotic Synechococcus RF-1. Curr Microbiol 27: 249–254Google Scholar
  46. Huang TC, Chen H-M, Pen S-Y and Chen T-H (1994) Biological clock in the prokaryote Synechococcus RF-1. Planta 193: 131– 136Google Scholar
  47. Johnson CH, Golden SS, Ishiura M and Kondo T (1996) Circadian clocks in prokaryotes. Mol Micro 21: 5–11Google Scholar
  48. Kok B, Forbush B and McGloin M(1970) Cooperation of charges in photosynthetic O2 evolution – 1. A linear four step mechanism. Photochem Photobiol 11: 457–475Google Scholar
  49. Kondo T, Strayer CA, Kulkarni RD, Taylor W, Ishiura M, Golden SS and Johnson CH (1993) Circadian rhythms in prokaryotes: Luciferase as a reporter of circadian gene expression in cyanobacteria. Proc Natl Acad Sci USA 90: 5672–5676Google Scholar
  50. Kondo T, Tsinoremas NF, Golden SS, Johnson CH, Kutsuna S and Ishiura M (1994) Circadian clock mutants of cyanobacteria. Science 266: 1233–1236Google Scholar
  51. Kretschmann H and Witt HT (1993) Chemical reduction of the water splitting enzyme system of photosynthesis and its lightinduced reoxidation characterized by optical and mass spectrometric measurements: A basis for the estimation of the states of the redox active manganese and of water in the quaternary oxygen-evolving S-state cycle. Biochim Biophys Acta 1144: 331–345Google Scholar
  52. Krieger A, Moya I and Weis E (1992) Energy-dependent quenching of chlorophyll-A fluorescence – effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and Photosystem II preparations. Biochim Biophys Acta 1102: 167–176Google Scholar
  53. Kruip J, Bald D, Boekema E and Rögner M (1994) Evidence for the existence of trimeric and monomeric Photosystem I complexes in thylakoid membranes from cyanobacteria. Photosynth Res 40: 279–286Google Scholar
  54. Lavorel J (1976) Matrix analysis of the oxygen evolving system of photosynthesis. J Theor Biol 57: 171–185Google Scholar
  55. Leon C, Kumazawa S and Mitsui A (1986) Cyclic appearance of aerobic nitrogenase activity during synchronous growth of unicellular cyanobacteria. Curr Microbiol 13: 149–153Google Scholar
  56. Liu Y, Tsinoremas NF, Johnson CH, Lebedeva, NV, Golden SS, Ishiura M and Kondo T (1995) Circadian orchestration of gene expression in cyanobacteria. Genes Dev 9: 1469–1478Google Scholar
  57. Liu Y, Tsinoremas NF, Golden SS, Kondo T and Johnson CH (1996) Circadian expression of genes involved in the purine biosynthetic pathway of the cyanobacterium Synechococcus sp. strain PCC 7942. Mol Microbiol 20: 1071–1081Google Scholar
  58. Merrick MJ (1992) Regulation of nitrogen fixation genes in freeliving and symbiotic bacteria. In: Stacey GG, Burris RH and Evans HJ. (eds) Biological Nitrogen Fixation, pp 835–876. Chapman and Hall, New YorkGoogle Scholar
  59. Messinger J and Renger G (1993) Generation, oxidation by the oxidized form of the tyrosine of polypeptide D2, and possible electronic configuration of the redox states S0, S-1, and S-2 of the water oxidase in isolated spinach thylakoids. Biochemistry 32: 9379–9386Google Scholar
  60. Messinger J, Seaton G, Wydzynski T, Wacker U and Renger g (1997) S-3 state of the water oxidase in Photosystem II. Biochemistry 36: 6862–6873Google Scholar
  61. Meunier PC (1993) O2 evolution by Photosystem II: The contribution of backward transitions to the anomalous behaviour of double-hits revealed by a new analysis method. Photosynth Res 36: 111–118Google Scholar
  62. Meunier PC and Popovic R (1991) Improvement of 4 sigma-analysis for the investigation of oxygen evolution by Photosystem-II. Photosynth Res 29: 113–115Google Scholar
  63. Meunier PC, Burnap RL and Sherman LA (1995a) Interaction of the photosynthetic and respiratory electron transport chains producing slow O2 signals under flashing light in Synechocystis sp. PCC 6803. Photosynth Res 45: 31–40Google Scholar
  64. Meunier PC, Watters JW, Colón-López MS and Sherman LA (1995b) Regulation of the O2-evolving mechanism during N2 fixation in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. In: Mathis P (ed) Research in Photosynthesis, Vol 2, pp 389–392. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  65. Meunier PC, Burnap RL and Sherman LA (1996) Improved 5-step modeling of the photosystem II S-state mechanism in cyanobacteria. Photosynth Res 47: 61–76Google Scholar
  66. Meunier PC, Colón-López MS and Sherman LA (1997) Temporal changes in state transitions and photosystem organization in the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Plant Physiol 115: 991–1000Google Scholar
  67. Meunier PC, Colón-López MS and Sherman LA (1998) Photosystem II cyclic heterogeneity and photoactivation in the diazotrophic, unicellular cyanobacterium Cyanothece sp. ATCC 51142. Plant Physiol 116: 1551–1562Google Scholar
  68. Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1992) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 33: 1233–1237Google Scholar
  69. Mi HL, Endo T, Ogawa T and Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36: 661–668Google Scholar
  70. Misra HS and Desai TS (1993) Involvement of acceptor side components of PS II in the regulatory mechanism of Plectonema boryanum grown photoautotrophically under diazotrophic condition. Biochem Biophys Res Com 194: 1001–1007Google Scholar
  71. Misra HS and Tuli R (1993) Photosystem II independent carbon dioxide fixation in Plectonema boryanum during photoautotrophic growth under nitrogen fixation conditions. J Plant Biochem Biotechnol 2: 101–104Google Scholar
  72. Misra HS and Tuli R (1994) Nitrogen fixation by Plectonema boryanum has a Photosystem II independent component. Microbiology 140: 971–976Google Scholar
  73. Mitsui, A, Kumazawa S, Takahashi A, Ikemoto, H, Cao S and Arai T (1986) Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323: 720–722Google Scholar
  74. Mitsui A, Cao S, Takahashi A and Arai T (1987) Growth synchrony and cellular parameters of the unicellular nitrogen-fixing marine cyanobacterium, Synechococcus sp. strain Miami BG043511 under continuous illumination. Physiol Plant 69: 1–8Google Scholar
  75. Mori T, Biner B and Johnson CH (1996) Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. Proc Natl Acad Sci USA 93: 10183–10188Google Scholar
  76. Mullineaux CW and Allen JF (1990) State 1-state 2 transitions in the cyanobacterium Synechococcus 6301 are controlled by the redox state of electron carriers between Photosystems I and II. Photosynth Res 23: 297–311Google Scholar
  77. Mullineaux CW, Tobin MJ and Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390: 421–424Google Scholar
  78. Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172: 242–251Google Scholar
  79. Peltier G, Ravenel J and Verméglio A (1987) Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: Evidence for a chlororespiration. Biochim Biophys Acta 893: 83–90Google Scholar
  80. Reddy KJ, Haskell JB, Sherman DM and Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175: 1284–1292Google Scholar
  81. Rögner M, Boekema EJ and Barber J (1996) How does Photosystem 2 split water? The structural basis of efficient energy conversion. TIBS 21: 44–49Google Scholar
  82. Schluchter WM, Shen G, Zhao J and Bryant DA (1996) Characterization of psaI and psaL mutants of Synechococcus sp. strain PCC 7002: A new model for state transitions in cyanobacteria. Photochem Photobiol 64: 53–66Google Scholar
  83. Schneegurt MA, Sherman DM, Nayar S and Sherman LA (1994) Oscillating behavior of carbohydrate granule formation and nitrogen fixation in the cyanobacterium, Cyanothece sp. ATCC 51142. J Bacteriol 176: 1586–1597Google Scholar
  84. Schneegurt MA, Sherman DM and Sherman LA (1997) Composition of the carbohydrate granules of the cyanobacterium, Cyanothece sp. ATCC 51142. Arch Microbiol 167: 89–98Google Scholar
  85. Shen G and Bryant DA (1995) Characterization of a Synechococcus sp. strain PCC 7002 mutant lacking Photosystem I. Protein assembly and energy distribution in the absence of the Photosystem I reaction center core complex. Photosynth Res 44: 41–53Google Scholar
  86. Simon RD (1971) Cyanophycin granules from the blue-green alga Anabaena cylindrica: A reserve material consisting of copolymers of aspartic acid and arginine. Proc Natl Acad Sci 68: 265–267Google Scholar
  87. Simon RD (1987) Inclusion bodies in the cyanobacteria: Cyanophycin, polyphosphate, polyhedral bodies. In: Fay P and Van Baalen C (eds) pp 70–76. The Cyanobacteria. Elsevier, Amsterdam/New York/OxfordGoogle Scholar
  88. Tsinoremas NF, Ishiura M, Kondo T, Andersson CR, Tanaka K, Takahashi H, Johnson CH and Golden SS (1996) A sigma factor that modifies the circadian expression of a subset of genes in cyanobacteria. EMBO J 15: 2488–2495Google Scholar
  89. Tuli R, Naithani S and Misra HS (1996) Cyanobacterial photosynthesis and the problem of oxygen in nitrogen-fixation: A molecular genetic view. J Sci Indust Res 55: 638–657Google Scholar
  90. Vermaas WFJ, Shen G and Styring S (1994) Electrons generated by Photosystem II are utilized by an oxidase in the absence of Photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 337: 103–108Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Louis A. Sherman
    • 1
  • Pascal Meunier
    • 1
  • Milagros S. Colón-López
    • 2
  1. 1.Department of Biological SciencesWest LafayetteUSA
  2. 2.Abbott Laboratories, Hospital Products DivisionUSA

Personalised recommendations