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Reexamining the Validity of the Z-Scheme: Is Photosystem I Required for Oxygenic Photosynthesis in Chlamydomonas?

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The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 7))

Summary

The ‘Z-scheme’ is the prevailing model for photosynthetic electron transport, in which electrons from Photosystem II (PS II) are transferred to Photosystem I (PS I) with the participation of the plastoquinone pool, the cytochrome b 6 f complex, and plastocyanin. PS II can accomplish water oxidation due to the low potential of its oxidized primary donor, and PS I reduces ferredoxin by virtue of its low potential iron-sulfur centers. There have been several claims over the last two decades that PS II can carry out the reduction of ferredoxin, lately using Chlamydomonas reinhardtii mutants defective in synthesis of PS I (Greenbaum et al., 1995; Lee et al., 1996). However, recent studies performed on mutants harboring deletions of genes encoding PS I subunits demonstrated that photoautotrophic growth and CO2 fixation require the presence of PS I (Cournac et al., 1997). When observed in ‘PS I-deficient’ mutants, photoautotrophic growth and CO2 fixation are most likely attributable to small amounts of PS I in those mutants. We discuss thermodynamic and evolutionary implications of the Z-scheme and possible exceptions to it.

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Abbreviations

CCCP:

carbonyl cyanide-m-chlorophenylhydrazone

Cyt:

cytochrome

DCMU:

3-(3,4-dichlorophenyl)-1,1-dimethylurea

DBMIB:

2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone

FCCP:

carbonyl cyanide-p-trifluorometh- oxyphenylhydrazone

Fd:

ferredoxin

FNR:

ferredoxin

NADP+:

reductase

OEC:

oxygen evolving complex

PC:

plastocyanin

PQ:

plastoquinone

PS I:

Photosystem I

PS II:

Photosystem II

RC:

reaction center

RC1:

reaction center of type 1 (quinone)

RCII:

reaction center of type 2 (Fe-S)

SQR:

sulflde:quinone oxidoreductase

References

  • Albertsson P-Å, Hsu BD, Tang GMS and Arnon DI (1983) Photosynthetic electron transport from water to NADP+ driven by Photosystem II in inside-out chloroplast vesicles. Proc Natl Acad Sci USA 80:3971–3975

    CAS  Google Scholar 

  • Amesz J (1995) The antenna-reaction center complex from heliobacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 687–697. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Arieli B, Shahak Y, Taglicht D, Hauska G and Padan E (1994) Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J Biol Chem 269:5705–5711

    CAS  PubMed  Google Scholar 

  • Arnon DI (1995) Divergent pathways of photosynthetic electron transfer: The autonomous oxygenic and anoxygenic photosystems. Photosynth Res 46:47–71

    Article  CAS  Google Scholar 

  • Arnon DI and Barber J (1990) Photoreduction of NADP+ by isolated reaction centers of Photosystem II: Requirement for plastocyanin. Proc Natl Acad Sci USA 87:5930–5934

    CAS  PubMed  Google Scholar 

  • Arnon DI, Tsujimoto HY and Tang GM (1980a) Contrasts between oxygenic and anoxygenic photoreduction of ferredoxin: Incompatibilities with prevailing concepts of photosynthetic electron transport. Proc Natl Acad Sci USA 77:2676–2680

    CAS  Google Scholar 

  • Arnon DI, Tsujimoto HY and Tang GM (1980b) Photoreduction of ferredoxin by chloroplasts with or without an accompanying photoreduction of the bound iron-sulfur centers. FEBS Lett 120:119–124

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Bennoun P and Levine RP (1967) Detecting mutants that have impaired photosynthesis by their increased level of fluorescence. Plant Physiol 42:1284–1287

    Google Scholar 

  • Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33:91–111

    Article  CAS  PubMed  Google Scholar 

  • Boichenko VA (1996) Can Photosystem II be a photogenerator of low potential reductant for CO2 fixation and O2 evolution? Photosynth Res 47:291–292

    Article  CAS  Google Scholar 

  • Boyer PD (1993) The binding change mechanism for ATP synthase—some probabilities and possibilities. Biochim Biophys Acta 1140:215–250

    CAS  PubMed  Google Scholar 

  • Brune DC (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 847–870. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Ann Rev Plant Physiol 31:341–374

    CAS  Google Scholar 

  • Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kück U, Bennoun P and Rochaix JD (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52:903–913

    Article  CAS  PubMed  Google Scholar 

  • Cohen Y, Jørgensen BB, Padan E and Shilo M (1975a) Sulphide-dependent anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. Nature 257:489–491

    Article  CAS  Google Scholar 

  • Cohen Y, Padan E and Shilo M (1975b) Facultative anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. J. Bact. 123:855–861

    CAS  PubMed  Google Scholar 

  • Cournac L, Redding K, Bennoun P and Peltier G (1997) Limited photosynthetic electron flow but no CO2 fixation in Chlamydomonas mutants lacking Photosystem I. FEBS Lett 416:65–68

    Article  CAS  PubMed  Google Scholar 

  • Crofts AR, Meinhardt SW, Jones KR and Snozzi M (1983) The role of the quinone pool in the cyclic electron transfer chain of Rhodopseudomonas sphaeroides. A modified Q-cycle mechanism. Biochim Biophys Acta 723:202–218

    CAS  Google Scholar 

  • Deisenhofer J and Michel H (1989) Nobel lecture. The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J 8:2149–2170

    CAS  PubMed  Google Scholar 

  • Duysens LNM, Amesz J and Kamp BM (1961) Two photochemical systems in photosynthesis. Nature 190:510–511

    CAS  PubMed  Google Scholar 

  • Ehrenreich A and Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 60:4517–4526

    CAS  PubMed  Google Scholar 

  • Emerson R (1958) The quantum yield of photosynthesis. Ann Rev Plant Physiol 9:1–24

    CAS  Google Scholar 

  • Feiler U and Hauska G (1995) The reaction center from green sulfur bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 665–685. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Fischer N and Stampacchia O, Redding K, Rochaix JD (1996) Selectable marker recycling in the chloroplast. Mol Gen Genet 251:373–380

    CAS  PubMed  Google Scholar 

  • Fischer N and Sétif P, Rochaix JD (1997) Targeted mutations in the psaC gene of Chlamydomonas reinhardtii: Preferential reduction of FB at low temperature is not accompanied by altered electron flow from Photosystem I to ferredoxin. Biochemistry 36:93–102

    Article  CAS  PubMed  Google Scholar 

  • Gaffron H (1939) Reduction of carbon dioxide with molecular hydrogen in green algae. Nature 143:240–205

    Google Scholar 

  • Gaffron H and Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol. 26:219–240

    CAS  Google Scholar 

  • Garlick S, Oren A and Padan E (1977) Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria. J Bacteriol 129:623–629

    CAS  PubMed  Google Scholar 

  • Gfeller RP and Gibbs M (1984) Fermentative metabolism of Chlamydomonas reinhardtii. I. Analysis of fermentative products from starch in dark and light. Plant Physiol 75:212–218

    CAS  Google Scholar 

  • Girard J, Chua NH, Bennoun P, Schmidt G and Delosme M (1980) Studies on mutants deficient in the Photosystem I reaction centers in Chlamydomonas reinhardtii. Curr Genet 2:215–221

    Article  CAS  Google Scholar 

  • Girard-Bascou J (1987) Mutations in four chloroplast loci of Chlamydomonas reinhardtii affecting the Photosystem I reaction centers. Curr Genet 12:483–488

    Article  CAS  Google Scholar 

  • Girard-Bascou J, Choquet Y, Schneider M, Delosme M and Dron M (1987) Characterization of a chloroplast mutation in the psaA2 gene of Chlamydomonas reinhardtii. Curr Genet 12:489–495

    Article  CAS  PubMed  Google Scholar 

  • Givan AL and Levine RP (1967) The photosynthetic electron transport chain of Chlaymdomonas reinhardtii. VII. Photosynthetic phosphorylation by a mutant strain of Chlaymdomonas reinhardtii deficient in activeP700. Plant Physiol 42:1264–1268

    CAS  PubMed  Google Scholar 

  • Golbeck JH (1993) Shared thematic elements in photochemical reaction centers. Proc Natl Acad Sci USA 90:1642–1646

    CAS  PubMed  Google Scholar 

  • Golbeck JH and Bryant DA (1991) Photosystem I. In: Lee CP (ed) Current Topics in Bioenergetics: Light Driven Reactions in Bioenergetics, Vol 16, pp 83–177. Academic Press, New York

    Google Scholar 

  • Goldschmidt-Clermont M, Girard-Bascou J, Choquet Y and Rochaix JD (1990) Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet 223:417–425

    Article  CAS  PubMed  Google Scholar 

  • Graves DA, Tevault CV and Greenbaum E (1989) Control of photosynthetic reductant: The role of light and temperature on sustained hydrogen photoevolution by Chlamydomonas sp. in an anoxic, carbon dioxide-containing atmosphere. Photochem Photobiol 50:571–576

    CAS  Google Scholar 

  • Greenbaum E (1984) Biophotolysis of water: The light saturation curves. Photobiochem Photobiophys 8:323–332

    CAS  Google Scholar 

  • Greenbaum E, Lee JW, Tevault CV, Blankenship SL and Mets LJ (1995) CO2 fixation and photoevolution of H2 and O2 in a mutant of Chlamydomonas lacking Photosystem I. Nature 376:438–441

    Article  CAS  Google Scholar 

  • Greenbaum E, Lee JW, Blankenship SL and Tevauit CV (1997) Hydrogen and oxygen production in mutant FUD26 of Chlamydomonas reinhardtii. Proceedings of the 1997 U.S. DOE Hydrogen Program Annual Technical Review: 1–10

    Google Scholar 

  • Haehnel W (1984) Photosynthetic electron transport in higher plants. Ann Rev Plant Physiol 35:659–693

    CAS  Google Scholar 

  • Happe T and Naber JD (1993) Isolation, characterization, and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214:475–481

    Article  CAS  PubMed  Google Scholar 

  • Harris EH (1989) The Chlamydomonas sourcebook. A comprehensive guide to biology and laboratory use. Academic Press, San Diego

    Google Scholar 

  • Healey FP (1970) The mechanism of hydrogen evolution by Chlamydomonas moewusii. Plant Physiol 45:153–159

    CAS  Google Scholar 

  • Hill R and Bendall F (1960) Function of the two cytochrome components inchloroplasts: Aworkinghypothesis. Nature 186:136–137

    CAS  Google Scholar 

  • Hoober JK (1984) Chloroplasts. Plenum Press, New York

    Google Scholar 

  • Hosier JP and Yocum CF (1985) Evidence for two cyclic photophosphorylation reactions concurrent with ferredoxin-catalyzed non-cyclic electron transport. Biochim Biophys Acta 808:21–31

    Google Scholar 

  • Hosier JP and Yocum CF (1987) Regulation of cyclic photophosphorylation during ferredoxin-mediated electron transport: effect of DCMU and the NADPH/NADP+ ratio. Plant Physiol 83:965–969

    Google Scholar 

  • Klimov VV and Krasnovsky AA (1982) Pheophytin participation in primary processes of electron transfer in Photosystem II reaction centers. Biofizika 27:179–89

    CAS  PubMed  Google Scholar 

  • Klimov VV, Klevanik AV, Shuvalov VA and Krasnovsky AA (1977) Reduction of pheophytin in the primary light reaction of Photosystem II. FEBS Lett 82:183–186

    Article  CAS  PubMed  Google Scholar 

  • Klimov VV, Allakhverdiev SI, Ladygin VG (1986) Photo-reduction of pheophytin in Photosystem II of the whole cells of green algae and cyanobacteria. Photosynth Res 10:355–361

    Article  CAS  Google Scholar 

  • Kück U, Choquet Y, Schneider M, Dron M and Bennoun P (1987) Structural and transcriptional analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardtii: Evidence for in vivo trans-splicing. EMBO J. 6:2185–2192

    PubMed  Google Scholar 

  • Lavergne J and Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Biochem Sci 16:129–134

    Article  CAS  PubMed  Google Scholar 

  • Lavergne J and Joliot P (1996) Dissipation in bioenergetic electron transfer chains. Photosynth Res 48:127–138

    Article  CAS  Google Scholar 

  • Lee JW, Tevault CV, Owens TG and Greenbaum E (1996) Oxygenic photoautotrophic growth without Photosystem I. Science 273:364–367

    CAS  PubMed  Google Scholar 

  • Levine RP (1968) Genetic dissection of photosynthesis. Science 162:768–771

    CAS  PubMed  Google Scholar 

  • Maione TE and Gibbs M (1986) Hydrogenase-mediated activities in isolated chloroplasts of Chlamydomonas reinhardii. Plant Physiol 80:360–363

    CAS  Google Scholar 

  • Myers J (1971) Enhancement studies in photosynthesis. Ann Rev Plant Physiol 22:289–312

    CAS  Google Scholar 

  • Nitschke W, Mattioli T and Rutherford AW (1996) The FeS-type photosystems and the evolution of photosynthetic reaction centers. In: Baltscheffsky H (ed) Origin and Evolution of Biological Energy Conversion, pp 177–203. VCH Publishers, New York

    Google Scholar 

  • Peltier G and Thibault P (1988) Oxygen-exchange studies in Chlamydomonas mutants deficient in photosynthetic electron transport: evidence for a Photosystem II-dependent oxygen uptake in vivo. Biochim Biophys Acta 936:319–324

    CAS  Google Scholar 

  • Ravenel J, Peltier G and Havaux M (1994) The cyclic electron pathways around Photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193:251–259

    Article  CAS  Google Scholar 

  • Russel GK and Gibbs M (1968) Evidence for the participation of the reductive pentose phosphate cycle in photoreduction and the oxyhydrogen reaction. Plant Physiol 43:649–652

    Google Scholar 

  • Rutherford AW and Nitschke W (1996) Photosystem II and the quinone-iron-containing reaction centers: comparisons and evolutionary perspectives. In: Baltscheffsky H (ed) Origin and Evolution of Biological Energy Conversion, pp 143–175. VCH Publishers, New York

    Google Scholar 

  • Schütz M, Shahak Y, Padan E and Hauska G (1997) Sulfide-quinone reductase from Rhodobacter capsulatus. Purification, cloning, and expression. J Biol Chem 272:9890–9894

    PubMed  Google Scholar 

  • Sétif PQ and Bottin H (1994) Laser flash absorption spectroscopy study of ferredoxin reduction by Photosystem I in Synechocystis sp. PCC 6803: Evidence for submicrosecond and microsecond kinetics. Biochemistry 33:8495–504

    PubMed  Google Scholar 

  • Sétif PQ and Bottin H (1995) Laser flash absorption spectroscopy study of ferredoxin reduction by Photosystem I: Spectral and kinetic evidence for the existence of several Photosystem I-ferredoxin complexes. Biochemistry 34:9059–9070

    PubMed  Google Scholar 

  • Shahak Y, Arieli B, Binder B and Padan E (1987) Sulfide-dependent photosynthetic electron flow coupled to proton translocation in thylakoids of the cyanobacterium Oscillatoria limnetica. Arch Biochem Biophys 259:605–615

    Article  CAS  PubMed  Google Scholar 

  • Shahak Y, Arieli B, Padan E and Hauska G (1992) Sulfide quinone reductase (SQR) activity in Chlorobium. FEBS Lett 299:127–130

    Article  CAS  PubMed  Google Scholar 

  • Slovacek RE, Crowther D and Hind G (1980) Relative activities of linear and cyclic electron flows during chloroplast CO2 fixation, Biochim Biophys Acta 592:495–505

    CAS  PubMed  Google Scholar 

  • Smart LB, Anderson SL and McIntosh L (1991) Targeted genetic inactivation of the Photosystem I reaction center in the cyanobacterium Synechocystis sp. PCC 6803. EMBO J. 10:3289–3296

    CAS  PubMed  Google Scholar 

  • Spreitzer RJ and Mets L (1981) Photosynthesis-deficient mutants of Chlamydomonas reinhardtii with associated light-sensitive phenotypes. Plant Physiol 67:565–569

    CAS  Google Scholar 

  • Staehelin LA, De Witt M (1984) Correlation of structure and function of chloroplast membranes at the supramolecular level. J Cell Biochcm 24:261–269

    CAS  Google Scholar 

  • Stryer L (1995) Biochemistry, Fourth Edition. W. H. Freeman and Company, New York

    Google Scholar 

  • Stuart TS and Gaffron H (1972a) The mechanism of hydrogen production by several algae. I. The effect of inhibitors of photophosphorylation. Planta 106:91–100

    CAS  Google Scholar 

  • Stuart TS and Gaffron H (1972b) The mechanism of hydrogen production by several algae. II. The contribution of Photosystem II. Planta 106:101–112

    CAS  Google Scholar 

  • Tagawa K, Tsujimoto HY and Arnon DI (1963) Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. Proc Natl Acad Sci USA 49:567–572

    CAS  PubMed  Google Scholar 

  • Takahashi Y, Matsumoto H, Goldschmidt-Clermont M and Rochaix JD (1994) Directed disruption of the Chlamydomonas chloroplast psbK gene destabilizes the Photosystem II reaction center complex. Plant Mol Biol 24:779–788

    Article  CAS  PubMed  Google Scholar 

  • Toelge M, Ziegler K, Maldener I and Lockau W (1991) Directed mutagenesis of the gene psaB of Photosystem I of the cyanobacterium Anabaena variabilis ATCC 29413. Biochim Biophys Acta 1060:233–236

    CAS  Google Scholar 

  • Togasaki RK and Whitmarsh J (1986) Multidisciplinary research in photosynthesis: A casehistory based on the green alga Chlamydomonas. Photosynth Res 10:415–122

    Article  CAS  Google Scholar 

  • Trebst A (1974) Energy conservation in photosynthetic electron transport of chloroplasts. Ann Rev Plant Physiol 25:423–458

    CAS  Google Scholar 

  • Vermaas WF, 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

    Article  CAS  PubMed  Google Scholar 

  • Webber AN, Su H, Bingham SE, Kaß H, Krabben L, Kuhn M, Jordan R, Schlodder E and Lubitz W (1996) Site-directed mutations affecting the spectroscopic characteristics and midpoint potential of the primary donor in Photosystem I. Biochemistry 35:12857–12863

    Article  CAS  PubMed  Google Scholar 

  • Willeford K.O, Gombos Z and Gibbs M (1989) Evidence for chloroplastic succinate dehydrogenase participating in the chloroplastic respiratory and photosynthetic electron transport chains in Chlamydomonas reinhardtii. Plant Physiol 90:1084–1087

    CAS  Google Scholar 

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Redding, K., Peltier, G. (1998). Reexamining the Validity of the Z-Scheme: Is Photosystem I Required for Oxygenic Photosynthesis in Chlamydomonas?. In: Rochaix, J.D., Goldschmidt-Clermont, M., Merchant, S. (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Advances in Photosynthesis and Respiration, vol 7. Springer, Dordrecht. https://doi.org/10.1007/0-306-48204-5_18

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  • DOI: https://doi.org/10.1007/0-306-48204-5_18

  • Publisher Name: Springer, Dordrecht

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