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

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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.

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References

  • Allen MM(1988) Inclusions: Cyanophycin. Methods Enzymol 167: 207–213

  • Allen MM and Weathers, PJ (1980) Structure and composition of cyanophycin granules in the cyanobacterium Aphanocapsa 6308. J Bacteriol 141: 959–962

    Google Scholar 

  • Apte SK (1996) Inter-relationship between photosynthesis and nitrogen fixation in cyanobacteria. J Sci Indust Res 55: 583–595

    Google Scholar 

  • 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: 778–792

    Google Scholar 

  • 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: 103–118

    Google Scholar 

  • Bendall DS and Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229: 23–38

    Google Scholar 

  • Bergman B, Gallon JR, Rai AN and Stal LJ (1997) N2-fixation by non-heterocystous cyanobacteria. FEMSMicrobiol Rev 19: 139– 185

    Google Scholar 

  • 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: 224–233

    Google Scholar 

  • 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: 66–73

    Google Scholar 

  • Buikema WJ and Haselkorn R (1993) Molecular genetics of cyanobacterial development. Annu Rev Plant Physiol Plant Mol Biol 44: 33–52

    Google Scholar 

  • 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: 440–446

    Google Scholar 

  • 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: 7404–7410

    Google Scholar 

  • 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: 874–882

    Google Scholar 

  • 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: 221–230

    Google Scholar 

  • 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: 1293–1298

    Google Scholar 

  • 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: 131–144

    Google Scholar 

  • Chen TH, Pen SY and Huang TC (1993) Induction of nitrogen-fixing circadian-rhythm Synechococcus RF-1 by light signals. Plant Sci 92: 179–182

    Google Scholar 

  • Cheniae GM and Martin IF (1972) Effects of hydroxylamine on Photosystem II. II. Photoreversal of the NH2OH destruction of O2 evolution. Plant Physiol 50: 87–94

    Google Scholar 

  • 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, Stuttgart

    Google Scholar 

  • 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: 4319–4327

    Google Scholar 

  • 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: 519–526

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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: 247–258

    Google Scholar 

  • 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: 227–244

    Google Scholar 

  • Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56: 340–373

    Google Scholar 

  • Gallon JR (1981) The oxygen sensitivity of nitrogenase: A problem for biochemists and microorganisms. TIBS 6: 9–23

    Google Scholar 

  • Gallon JR (1992) Tansley Review No. 44. Reconciling the incompatible: N2 fixation and O2. New Phytol 122: 571–609

    Google Scholar 

  • Gallon JR and Chaplin AE (1987) An Introduction to Nitrogen Fixation. Cassell, London, UK

    Google Scholar 

  • 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: 6847–6856

    Google Scholar 

  • 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: 2789–2798

    Google Scholar 

  • Golden SS, Ishiura M, Johnson CH and Kondo T (1997) Cyanobacterial circadian rhythms. Annu Rev Plant Physiol Plant Mol Biol 48: 327–354

    Google Scholar 

  • Grobbelaar N, Huang TC, Lin HY and Chow TJ (1986) Dinitrogen fixing endogenous rhythm in Synechococcus RF1. FEMS Microbiol Lett 37: 173–177

    Google Scholar 

  • 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: 29–33

    Google Scholar 

  • Haselkorn R (1978) Heterocysts. Annu Rev Plant Physiol 29: 319– 344

    Google Scholar 

  • Haselkorn R (1986) Organization of the genes for nitrogen fixation in photosynthetic bacteria and cyanobacteria. Annu Rev Microbiol 40: 525–547

    Google Scholar 

  • Haselkorn R (1992) Developmentally regulated gene rearrangements in prokaryotes. Annu Rev Genet 26: 113–130

    Google Scholar 

  • 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 York

    Google Scholar 

  • Hirano M, Satoh K and Katoh S (1980) Plastoquinone as a common link between photosynthesis and respiration in blue-green alga. Photosynth Res 1: 149–162

    Google Scholar 

  • Howard JB and Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96: 2965–2982

    Google Scholar 

  • Huang TC and Chow TJ (1986) New type of N2-fixing unicellular cyanobacterium (blue-green alga). FEMS Microbiol Lett 36: 109–110

    Google Scholar 

  • 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: 324–326

    Google Scholar 

  • 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: 127–130

    Google Scholar 

  • Huang TC, Tu J, Chow TJ and Chen TH (1990) Circadian rhythm of the prokaryote Synechococcus sp. RF1. Plant Physiol 92: 531– 533

    Google Scholar 

  • 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: 129–133

    Google Scholar 

  • Huang T-C, Wang S-T and Grobbelaar N (1993) Circadian rhythm mutants of the prokaryotic Synechococcus RF-1. Curr Microbiol 27: 249–254

    Google Scholar 

  • Huang TC, Chen H-M, Pen S-Y and Chen T-H (1994) Biological clock in the prokaryote Synechococcus RF-1. Planta 193: 131– 136

    Google Scholar 

  • Johnson CH, Golden SS, Ishiura M and Kondo T (1996) Circadian clocks in prokaryotes. Mol Micro 21: 5–11

    Google Scholar 

  • Kok B, Forbush B and McGloin M(1970) Cooperation of charges in photosynthetic O2 evolution – 1. A linear four step mechanism. Photochem Photobiol 11: 457–475

    Google Scholar 

  • 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: 5672–5676

    Google Scholar 

  • Kondo T, Tsinoremas NF, Golden SS, Johnson CH, Kutsuna S and Ishiura M (1994) Circadian clock mutants of cyanobacteria. Science 266: 1233–1236

    Google Scholar 

  • 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: 331–345

    Google Scholar 

  • 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: 167–176

    Google Scholar 

  • 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: 279–286

    Google Scholar 

  • Lavorel J (1976) Matrix analysis of the oxygen evolving system of photosynthesis. J Theor Biol 57: 171–185

    Google Scholar 

  • Leon C, Kumazawa S and Mitsui A (1986) Cyclic appearance of aerobic nitrogenase activity during synchronous growth of unicellular cyanobacteria. Curr Microbiol 13: 149–153

    Google Scholar 

  • 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: 1469–1478

    Google Scholar 

  • 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: 1071–1081

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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: 9379–9386

    Google Scholar 

  • Messinger J, Seaton G, Wydzynski T, Wacker U and Renger g (1997) S-3 state of the water oxidase in Photosystem II. Biochemistry 36: 6862–6873

    Google Scholar 

  • 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: 111–118

    Google Scholar 

  • Meunier PC and Popovic R (1991) Improvement of 4 sigma-analysis for the investigation of oxygen evolution by Photosystem-II. Photosynth Res 29: 113–115

    Google Scholar 

  • 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: 31–40

    Google Scholar 

  • 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 Netherlands

    Google Scholar 

  • Meunier PC, Burnap RL and Sherman LA (1996) Improved 5-step modeling of the photosystem II S-state mechanism in cyanobacteria. Photosynth Res 47: 61–76

    Google Scholar 

  • 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: 991–1000

    Google Scholar 

  • 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: 1551–1562

    Google Scholar 

  • 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: 1233–1237

    Google Scholar 

  • 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: 661–668

    Google Scholar 

  • 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: 1001–1007

    Google Scholar 

  • 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: 101–104

    Google Scholar 

  • Misra HS and Tuli R (1994) Nitrogen fixation by Plectonema boryanum has a Photosystem II independent component. Microbiology 140: 971–976

    Google Scholar 

  • 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: 720–722

    Google Scholar 

  • 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: 1–8

    Google Scholar 

  • 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: 10183–10188

    Google Scholar 

  • 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: 297–311

    Google Scholar 

  • Mullineaux CW, Tobin MJ and Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390: 421–424

    Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172: 242–251

    Google Scholar 

  • 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: 83–90

    Google Scholar 

  • Reddy KJ, Haskell JB, Sherman DM and Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175: 1284–1292

    Google Scholar 

  • Rögner M, Boekema EJ and Barber J (1996) How does Photosystem 2 split water? The structural basis of efficient energy conversion. TIBS 21: 44–49

    Google Scholar 

  • 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: 53–66

    Google Scholar 

  • 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: 1586–1597

    Google Scholar 

  • Schneegurt MA, Sherman DM and Sherman LA (1997) Composition of the carbohydrate granules of the cyanobacterium, Cyanothece sp. ATCC 51142. Arch Microbiol 167: 89–98

    Google Scholar 

  • 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: 41–53

    Google Scholar 

  • 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: 265–267

    Google Scholar 

  • 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/Oxford

    Google Scholar 

  • 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: 2488–2495

    Google Scholar 

  • 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: 638–657

    Google Scholar 

  • 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: 103–108

    Google Scholar 

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  1. Milagros S. Colón-López

    Present address: Abbott Laboratories, Hospital Products Division, Abbott Park, IL, 60064-3500, USA

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  1. Department of Biological Sciences, Lilly Hall of Life Sciences, nPurdue University, West Lafayette, IN, 47907-1392, USA

    Louis A. Sherman & Pascal Meunier

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Sherman, L.A., Meunier, P. & Colón-López, M.S. Diurnal rhythms in metabolism: A day in the life of a unicellular, diazotrophic cyanobacterium. Photosynthesis Research 58, 25–42 (1998). https://doi.org/10.1023/A:1006137605802

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