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Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae)

Abstract

Unicellular green algae have the ability to operate in two distinctly different environments (aerobic and anaerobic), and to photosynthetically generate molecular hydrogen (H2). A recently developed metabolic protocol in the green alga Chlamydomonas reinhardtii permitted separation of photosynthetic O2-evolution and carbon accumulation from anaerobic consumption of cellular metabolites and concomitant photosynthetic H2-evolution. The H2 evolution process was induced upon sulfate nutrient deprivation of the cells, which reversibly inhibits photosystem-II and O2-evolution in their chloroplast. In the absence of O2, and in order to generate ATP, green algae resorted to anaerobic photosynthetic metabolism, evolved H2 in the light and consumed endogenous substrate. This study summarizes recent advances on green algal hydrogen metabolism and discusses avenues of research for the further development of this method. Included is the mechanism of a substantial tenfold starch accumulation in the cells, observed promptly upon S-deprivation, and the regulated starch and protein catabolism during the subsequent H2-evolution. Also discussed is the function of a chloroplast envelope-localized sulfate permease, and the photosynthesis–respiration relationship in green algae as potential tools by which to stabilize and enhance H2 metabolism. In addition to potential practical applications of H2, approaches discussed in this work are beginning to address the biochemistry of anaerobic H2 photoproduction, its genes, proteins, regulation, and communication with other metabolic pathways in microalgae. Photosynthetic H2 production by green algae may hold the promise of generating a renewable fuel from nature’s most plentiful resources, sunlight and water. The process potentially concerns global warming and the question of energy supply and demand.

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Abbreviations

Chl:

Chlorophyll

DCMU:

3-(3′,4′-Dichlorophenyl)-1,1-dimethyl urea

LHC:

Light-harvesting complex

PS:

Photosystem

PAR:

Photosynthetically active radiation

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

References

  1. Adams MWW (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020:115–145

    PubMed  CAS  Google Scholar 

  2. Adams MWW, Stiefel EI (2000) Organometallic iron: the key to biological hydrogen metabolism. Curr Opin Chem Biol 4:214–220

    PubMed  CAS  Google Scholar 

  3. Antal TK, Lindblad P (2005) Production of H-2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol 98:114–120

    PubMed  CAS  Google Scholar 

  4. Antal TK, Krendeleva TE, Rubin AB, Laurinavichene TV, Tsygankov AA, Makarova VV, Kosourov S, Ghirardi ML, Seibert M (2003) The dependence of algal H2 production on photosystem II and O2-consumption activity in sulfur-deprived Chlamydomonas reinhardtii cells. Biochim Biophys Acta 1607:153–160

    PubMed  CAS  Google Scholar 

  5. Appel J, Schulz R (1998) Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising?. J Photochem Photobiol B Biol 47:1–11

    CAS  Google Scholar 

  6. Arnon DI, Mitsui A, Paneque A (1961) Photoproduction of hydrogen gas coupled with photosynthetic phosphorylation. Science 134:1425

    Google Scholar 

  7. Ball S, Marianne T, Dirick L, Fresnoy M, Delrue B, Decq A (1991) A Chlamydomonas reinhardtii low-starch mutant is defective for 3-phosphoglycerate activation and orthophosphate inhibition of ADP-glucose pyrophosphorylase. Planta 185:17–26

    CAS  Google Scholar 

  8. Bamberger ES, King D, Erbes DL, Gibbs M (1982) H2 and CO2 evolution by anaerobically adapted Chlamydomonas reinhardtii F60. Plant Physiol 69:1268–1273

    PubMed  CAS  Google Scholar 

  9. Ben-Amotz A, Avron M (1990) The biotechnology of cultivating the halotolerant alga Dunaliella. Trends Biotechnol 8:121–128

    CAS  Google Scholar 

  10. Bennoun P (2001) Chlororespiration and the process of carotenoid biosynthesis. Biochim Biophys Acta 1506:133–142

    PubMed  CAS  Google Scholar 

  11. Bishop NI, Gaffron H (1963) On the interrelation of the mechanisms for oxygen and hydrogen evolution in adapted algae. In: Publ 1145, Photosynthetic mechanisms in green plants. Natl Acad Sci Natl Res Council, Washington, DC, pp 441–451

  12. Bishop NI, Frick M, Jones LW (1977) Photohydrogen production in green algae: water serves as the primary substrate for hydrogen and oxygen production. In: Mitsui A, Miyachi S, San Pietro A, Tamura S (eds) Biological solar energy conversion. Academic Press, New York, pp 3–22

    Google Scholar 

  13. Cao H, Zhang L, Melis A (2001) Bioenergetic and metabolic processes for the survival of sulfur-deprived Dunaliella salina (Chlorophyta). J Appl Phycol 13:25–34

    CAS  Google Scholar 

  14. Chen H-C, Melis A (2004) Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta 220:198–210

    PubMed  CAS  Google Scholar 

  15. Chen HC, Yokthongwattana K, Newton AJ, Melis A (2003) SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii. Planta 218:98–106

    PubMed  CAS  Google Scholar 

  16. Chen H-C, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H2 evolution in Chlamydomonas reinhardtii. Photosynth Res 84:289–296

    PubMed  CAS  Google Scholar 

  17. Cinco RM, Macinnis JM, Greenbaum E (1993) The role of carbon dioxide in light-activated hydrogen production by Chlamydomonas reinhardtii. Photosynth Res 38:27–33

    CAS  Google Scholar 

  18. Cournac L, Mus F, Bernard L, Guedeney G, Vignais P, Peltier G (2002) Limiting steps of hydrogen production in Chlamydomonas reinhardtii and Synechocystis PCC 6803 as analysed by light-induced gas exchange transients. Int J Hydrogen Energy 27:1229–1237

    CAS  Google Scholar 

  19. Dauvillée D, Chochois V, Steup M, Haebel S, Eckermann N, Ritte G, Ral JP, Colleoni C, Hicks G, Wattebled F, Deschamps P, d’Hulst C, Liénard L, Cournac L, Putaux JL, Dupeyre D, Ball SG (2006) Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant J 48:274–285

    PubMed  Google Scholar 

  20. Davies JP, Yildiz F, Grossman AR (1994) Mutants of Chlamydomonas with aberrant responses to sulfur deprivation. Plant Cell 6:53–63

    PubMed  CAS  Google Scholar 

  21. Endo T, Shikanai T, Sato F, Asada K (1998) NAD(P)H dehydrogenase-dependent, antimycin A-sensitive electron donation to plastoquinone in tobacco chloroplasts. Plant Cell Physiol 39:1226–1231

    CAS  Google Scholar 

  22. Feild TS, Nedbal L, Ort DR (1998) Nonphotochemical reduction of the plastoquinone pool in sunflower leaves originates from chlororespiration. Plant Physiol 116:1209–1218

    PubMed  CAS  Google Scholar 

  23. Florin L, Tsokoglou A, Happe T (2001) A novel type of [Fe]-hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetical electron transport chain. J Biol Chem 276:6125–6132

    PubMed  CAS  Google Scholar 

  24. Forestier M, King P, Zhang LP, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 270:2750–2758

    PubMed  CAS  Google Scholar 

  25. Fouchard S, Hemschemeier A, Caruana A, Pruvost K, Legrand J, Happe T, Peltier G, Cournac L (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Appl Environ Microbiol 71:6199–6205

    PubMed  CAS  Google Scholar 

  26. Francis K, Senger H (1985) Correlation between respiration and hydrogenase adaptation in Scenedesmus obliquus. Physiol Plant 65:167–170

    CAS  Google Scholar 

  27. Gaffron H (1939) Reduction of CO2 with H2 in green plants. Nature 143:204–205

    CAS  Google Scholar 

  28. Gaffron H (1940) Carbon dioxide reduction with molecular hydrogen in green algae. Am J Bot 27:273–283

    CAS  Google Scholar 

  29. Gaffron H (1942) Reduction of carbon dioxide coupled with the oxyhydrogen reaction in algae. J Gen Physiol 26:241–267

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  32. Ghirardi ML, Togasaki RK, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotech 63:141–151

    Article  Google Scholar 

  33. Ghirardi ML, Zhang L, Lee JW, Flynn T, Seibert M, Greenbaum E, Melis A (2000) Microalgae: a green source of renewable H2. Trends Biotechnol 18:506–511

    PubMed  CAS  Google Scholar 

  34. Gibbs M, Gfeller RP, Chen C (1986) Fermentative metabolism of Chlamydomonas reinhardtii. III. Photo-assimilation of acetate. Plant Physiol 82:160–166

    PubMed  CAS  Google Scholar 

  35. Giordano M, Pezzoni V, Hell R (2000) Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol 124:857–864

    PubMed  CAS  Google Scholar 

  36. Girbal L Von Abendroth G Winkler M, Benton BMC, Meynial-Salles I Croux C, Peters JW, Happe T, Soucaille P (2005) Homologous and heterologous overexpression in Clostridium acetobutylicum and characterization of purified clostridial and algal Fe-only hydrogenases with high specific activities. Appl Environ Microbiol 71:2777–2781

    Google Scholar 

  37. Godde D, Trebst A (1980) NADH as electron donor for the photosynthetic membrane of Chlamydomonas reinhardtii. Arch Microbiol 127:245–252

    CAS  Google Scholar 

  38. Greenbaum E (1982) Photosynthetic hydrogen and oxygen production: kinetic studies. Science 196:879–880

    Google Scholar 

  39. Greenbaum E (1988) Energetic efficiency of H2 photoevolution by algal water-splitting. Biophys J 54:365–368

    CAS  PubMed  Google Scholar 

  40. Greenbaum E, Guillard RRL, Sunda WG (1983) Hydrogen and oxygen photoproduction by marine algae. Photochem Photobiol 37:649–655

    CAS  Google Scholar 

  41. Happe T, Kaminski A (2002) Differential regulation of the [Fe]-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269:1022–1032

    PubMed  CAS  Google Scholar 

  42. Happe T, 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

    PubMed  CAS  Google Scholar 

  43. Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. Eur J Biochem 222:769–774

    PubMed  CAS  Google Scholar 

  44. Hemschemeier A, Happe T (2005) The exceptional photofermentative hydrogen metabolism of the green alga Chlamydomonas reinhardtii. Biochem Soc Trans 33:39–41

    PubMed  CAS  Google Scholar 

  45. Hicks GR, Hironaka CM, Dauvillee D, Funke RP, d’Hulst C, Waffenschmidt S, Ball SG (2001) When simpler is better. Unicellular green algae for discovering new genes and functions in carbohydrate metabolism. Plant Physiol 127:1334–1338

    PubMed  CAS  Google Scholar 

  46. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular Cyanobacterium Synechocystis sp strain PCC6803. II Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    PubMed  CAS  Google Scholar 

  47. Kessler E (1966) The effect of glucose on hydrogenase activity in Chlorella. Biochim Biophys Acta 112:173–175

    PubMed  CAS  Google Scholar 

  48. Kessler E (1973) Effect of anaerobiosis on photosynthetic reactions and nitrogen metabolism of algae with and without hydrogenase. Arch Microbiol 93:91–100

    CAS  Google Scholar 

  49. Kessler E (1974) Hydrogenase, photoreduction and anaerobic growth of algae. In: Algal physiology and biochemistry. Blackwell, Oxford, pp 454–473

  50. Kessler E (1976) Microbial production and utilization of gases (H2, CH4, CO). In: Schlegel HG, Gottschalk G, Pfennig N (eds) Microbial production and utilization of gases. Akad Wiss Goltze, Göttingen, pp 247–254

    Google Scholar 

  51. King PW, Posewitz MC, Ghirardi ML, Seibert M (2006) Functional studies of [FeFe] hydrogenase maturation in an Escherichia coli biosynthetic system. J Bacteriol 188:2163–2172

    PubMed  CAS  Google Scholar 

  52. Kohn C, Schumann J (1993) Nucleotide sequence and homology comparison of two genes of the sulfate transport operon from the cyanobacterium Synechocystis sp. PCC6803. Plant Mol Biol 21:409–412

    PubMed  CAS  Google Scholar 

  53. Kosourov S, Seibert M, Ghirardi ML (2003) Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures. Plant Cell Physiol 44:146–155

    PubMed  CAS  Google Scholar 

  54. Kosourov S, Patrusheva E, Ghirardi ML, Seibert M, Tsygankov A (2007) A comparison of hydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii under different growth conditions J Biotech 128:776–787

    CAS  Google Scholar 

  55. Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H-2 production in engineered green algal cells. J Biol Chem 280:34170–34177

    PubMed  CAS  Google Scholar 

  56. Kubicki A, Funk E, Westhoff P, Steinmuller K (1996) Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C-4 plant sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved. Planta 199:276–281

    CAS  Google Scholar 

  57. Kuroiwa H, Mori T, Takahara M, Miyagishima S, Kuroiwa T (2002) Chloroplast division machinery as revealed by immunofluorescence and electron microscopy. Planta 215:185–190

    PubMed  CAS  Google Scholar 

  58. Laudenbach DE, Grossman A (1991) Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: evidence for function in sulfate transport. J Bacteriol 173:2739–2750

    PubMed  CAS  Google Scholar 

  59. Ley AC, Mauzerall DC (1982) Absolute absorption cross sections for photosystem II and the minimum quantum requirement for photosynthesis in Chlorella vulgaris. Biochim Biophys Acta 680:95–106

    CAS  Google Scholar 

  60. Maione TE, Gibbs M (1986a) Association of the chlorplastic respiratory and photosynthetic electron transport chains of C. reinhardii with photoreduction and the oxyhydrogen reaction. Plant Physiol 80:364–368

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  62. McBride AC, Lien S, Togasaki RK, San Pietro A (1977) Mutational analysis of Chlamydomonas reinhardi: application to biological solar energy conversion. In: Mitsui A, Miyachi S, San Pietro A, Tamura S (eds) Biological solar energy conversion. Academic Press, New York, pp 77–86

    Google Scholar 

  63. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo?. Trends Plant Sci 4:130–135

    PubMed  Google Scholar 

  64. Melis A (2002) Green alga hydrogen production: progress, challenges and prospects. Int J Hydrogen Energy 27:1217–1228

    CAS  Google Scholar 

  65. Melis A, Chen HC (2005) Chloroplast sulfate transport in green algae: genes, proteins and effects. Photosynth Res 86:299–307

    PubMed  CAS  Google Scholar 

  66. Melis A, Happe T (2001) Hydrogen production: green algae as a source of energy. Plant Physiol 127:740–748

    PubMed  CAS  Google Scholar 

  67. Melis A, Neidhardt J, Benemann JR (1998) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10:515–525

    Google Scholar 

  68. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136

    PubMed  CAS  Google Scholar 

  69. Melis A, Seibert M, Happe T (2004) Genomics of green algal hydrogen research. Photosynth Res 82:277–288

    PubMed  CAS  Google Scholar 

  70. Meyer J, Gagnon J (1991) Primary structure of hydrogenase I from Clostridium pasterianum. Biochemistry 30:9697–9704

    PubMed  CAS  Google Scholar 

  71. Miyagishima S, Kuroiwa H, Kuroiwa T (2001) The timing and manner of disassembly of the apparatuses for chloroplast and mitochondrial division in the red alga Cyanidioschyzon merolae. Planta 212:517–528

    PubMed  CAS  Google Scholar 

  72. Mus F, Cournac L, Cardettini W, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H-2 photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708:322–332

    PubMed  CAS  Google Scholar 

  73. Neyland R, Urbatsch LE (1996) The ndhf chloroplast gene detected in all vascular plant divisions. Planta 200:273–277

    PubMed  CAS  Google Scholar 

  74. Ohyma K, Fukuzawa H, Kohchi T, Shirai H, Sano T, others (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574

    Google Scholar 

  75. Osteryoung KW, McAndrew RS (2001) The plastid division machine. Annu Rev Plant Physiol Plant Mol Biol 52:315–333

    PubMed  CAS  Google Scholar 

  76. Osteryoung KW, Pyke KA (1998) Plastid division: evidence for a prokaryotically derived mechanism. Curr Opin Plant Biol 1:475–479

    PubMed  CAS  Google Scholar 

  77. Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991–2004

    PubMed  CAS  Google Scholar 

  78. Peters JW (1999) Structure and mechanism of iron-only hydrogenases. Curr Opin Struct Biol 9:670–676

    PubMed  CAS  Google Scholar 

  79. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853–1858

    PubMed  CAS  Google Scholar 

  80. Polle JEW, Kanakagiri S, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217:49–59

    PubMed  CAS  Google Scholar 

  81. Posewitz MC, King PW, Smolinski SL, Zhang LP, Seibert M, Ghirardi ML (2004a) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711–25720

    PubMed  CAS  Google Scholar 

  82. Posewitz MC, Smolinski SL, Kanakagiri S, Melis A, Seibert M, Ghirardi ML (2004b) Hydrogen photoproduction is attenuated by disruption of an isoamylase gene in Chlamydomonas reinhardtii. Plant Cell 16:2151–2163

    PubMed  CAS  Google Scholar 

  83. Pyke KA (1997) The genetic control of plastid division in higher plants. Am J Bot 84:1017–1027

    CAS  Google Scholar 

  84. Pyke KA (1999) Plastid division and development. Plant Cell 11:549–556

    PubMed  CAS  Google Scholar 

  85. Randt C, Senger H (1985) Participation of the two photosystems in light dependent hydrogen evolution in Scenedesmus obliquus. Photochem Photobiol 42:553–557

    CAS  Google Scholar 

  86. Roessler PG, Lien S (1984) Activation and de novo synthesis of hydrogenase in Chlamydomonas. Plant Physiol 76:1086–1089

    PubMed  CAS  Article  Google Scholar 

  87. Rupprecht J, Hankamer B, Mussgnug JH, Ananyev G, Dismukes C, Kruse O (2006) Perspectives and advances of biological H-2 production in microorganisms. Appl Microbiol Biotechnol 72:442–449

    PubMed  CAS  Google Scholar 

  88. Sazanov LA, Burrows PA, Nixon PJ (1998) The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. Proc Natl Acad Sci USA 95:1319–1324

    PubMed  CAS  Google Scholar 

  89. Schnackenberg J, Schulz R, Senger H (1993) Characterization and purification of a hydrogenase from the eukaryotic green alga Scenedesmus obliquus. FEBS Lett 327:21–24

    PubMed  CAS  Google Scholar 

  90. Schulz R (1996) Hydrogenases and hydrogen production in eukaryotic organisms and cyanobacteria. J Mar Biotechnol 4:16–22

    CAS  Google Scholar 

  91. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    PubMed  CAS  Google Scholar 

  92. Smith BM, Morrissey PJ, Guenther JE, Nemson JA, Harrison MA, Allen JF, Melis A (1990) Response of the photosynthetic apparatus in Dunaliella salina (green algae) to irradiance stress. Plant Physiol 93:1433–1440

    PubMed  CAS  Google Scholar 

  93. Spruit CP (1958) Simultaneous photoproduction of hydrogen and oxygen by Chlorella. Meded Landbouwhogeschool Wageningen 58:1–17

    CAS  Google Scholar 

  94. Stuart TS, Gaffron H (1972) The mechanism of hydrogen photoproduction by several algae. II The contribution of photosystem II. Planta 106:101–112

    CAS  Google Scholar 

  95. Tetali S, Mitra M, Melis A (2007) Development of the light-harvesting chlorophyll antenna in the green alga Chlamydomonas reinhardtii is regulated by the novel Tla1 gene. Planta 225:813–829

    PubMed  CAS  Google Scholar 

  96. Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener A, Allahverdiyeva Y, Aro EM (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–793

    PubMed  Google Scholar 

  97. Tsygankov AA, Kosourov SN, Tolstygina IV, Ghirardi ML, Seibert M (2006) Hydrogen production by sulfur-deprived Chlamydomonas reinhardtii under photoautotrophic conditions. Int J Hydrogen Energy 31:1574–1584

    CAS  Google Scholar 

  98. Turmel M, Otis C, Lemieux C (1999) The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proc Natl Acad Sci USA 96:10248–10253

    PubMed  CAS  Google Scholar 

  99. Van den Koornhuyse N, Libessart N, Delrue B, Zabawinski C, Decq A, Iglesias A, Carton A, Preiss J, Ball S (1996) Control of starch composition and structure through substrate supply in the monocellular alga Chlamydomonas reinhardtii. J Biol Chem 271:16281–16287

    PubMed  Google Scholar 

  100. Vignais PN, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501

    PubMed  CAS  Google Scholar 

  101. Vitha S, McAndrew RS, Osteryoung KW (2001) FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153:111–119

    PubMed  CAS  Google Scholar 

  102. Voordouw G, Strang JD, Wilson FR (1989) Organization of the genes encoding (Fe) hydrogenase in Desulfovibrio vulgaris. J Bacteriol 171:3881–3889

    PubMed  CAS  Google Scholar 

  103. Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94:5967–5972

    PubMed  CAS  Google Scholar 

  104. White AL, Melis A (2006) Biochemistry of hydrogen metabolism in Chlamydomonas reinhardtii wild type and a Rubisco-less mutant. Int J Hydrogen Energy 31:455–464

    CAS  Google Scholar 

  105. Winkler M, Hemschemeier A, Gotor C, Melis A, Happe T (2002) [Fe]-hydrogenases in green algae: photo-fermentation and hydrogen evolution under sulfur deprivation. Intl J Hydrogen Energy 27:1431–1439

    CAS  Google Scholar 

  106. Wünschiers R, Stangier K, Senger H, Schulz R (2001a) Molecular evidence for a [Fe]-hydrogenase in the green alga Scenedesmus obliquus. Curr Microbiol 42:353–360

    PubMed  Google Scholar 

  107. Wünschiers R, Senger H, Schulz R (2001b) Electron pathways involved in H-2-metabolism in the green alga Scenedesmus obliquus. Biochim Biophys Acta 1503:271–278

    PubMed  Google Scholar 

  108. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron-transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139

    PubMed  CAS  Google Scholar 

  109. Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981–987

    PubMed  CAS  Google Scholar 

  110. Zabawinski C, Van den Koornhuyse N, d’Hulst C, Schlichting R, Giersch C, Delrue B, Lacroix JM, Preiss J, Ball S (2001) Starchless mutants of Chlamydomonas reinhardtii lack the small subunit of a heterotetrameric ADP-glucose pyrophosphorylase. J Bacteriol 183:1069–1077

    PubMed  CAS  Google Scholar 

  111. Zhang L, Melis A (2002) Probing green algal hydrogen production. Phil Trans R Soc Lond Biol Sci 357:1499–1509

    CAS  Google Scholar 

  112. Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561

    PubMed  CAS  Google Scholar 

  113. Zhang ZD, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryotic Cell 3:1331–1348

    PubMed  CAS  Google Scholar 

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Acknowledgments

Thanks are due to Dr. Hsu-Ching Chen for help with the measurement of H2-production in anti-sulP strains of C. reinhardtii.

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Correspondence to Anastasios Melis.

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Melis, A. Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226, 1075–1086 (2007). https://doi.org/10.1007/s00425-007-0609-9

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Keywords

  • Chlamydomonas reinhardtii
  • Green algae
  • Hydrogenase
  • H2
  • Hydrogen production
  • Photosynthesis
  • Sulfur deprivation