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Genomics of green algal hydrogen research

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Abstract

This article summarizes knowledge on genes and their respective proteins in the field of green algal hydrogen research. Emphasis is placed on recently cloned genes from the unicellular green alga Chlamydomonas reinhardtii, including HydA1 and HydA2, which encode homologous [Fe]-hydrogenases, Tla1, which encodes a chlorophyll antenna size regulatory gene, SulP, which encodes a chloroplast sulfate permease, and Sta7, which encodes an isoamylase. Analysis of the structure and function of these genes and of their respective proteins in C. reinhardtii, and related unicellular green algae, is presented in light of the role they play in the hydrogen metabolism in these organisms. A discussion is offered as to the potential application of these genes in the field of hydrogen photoproduction.

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References

  • MWW Adams (1990) ArticleTitleThe structure and mechanism of iron hydrogenases Biochim Biophys Acta 1020 115–145 Occurrence Handle2173950

    PubMed  Google Scholar 

  • TK Antal TE Krendeleva TV Laurinavichene VV Makarova AA Tsygankov M Seibert AB Rubin (2001) ArticleTitleThe relationship between photosystem 2 activity and hydrogen production in sulfur-deprived Chlamydomonas reinhardtii cells Doklady Akademii Nauk (Biochem Biophys) 381 371–375 Occurrence Handle10.1023/A:1013315310173

    Article  Google Scholar 

  • TK Antal TE Krendeleva AB Rubin TV Laurinavichene AA Tsygankov VV Makarova S Kosourov ML Ghirardi M Seibert (2003) ArticleTitleThe dependence of algal H2 production on photosystem II and O2-consumption activity in sulfur-deprived Chlamydomonas reinhardtii cells Biochim Biophys Acta 1607 153–160 Occurrence Handle14670605

    PubMed  Google Scholar 

  • J Appel R Schulz (1998) ArticleTitleHydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising? J Photochem Photobiol 47 1–11 Occurrence Handle10.1016/S1011-1344(98)00179-1

    Article  Google Scholar 

  • DI Arnon A Mitsui A Paneque (1961) ArticleTitlePhotoproduction of hydrogen gas coupled with photosynthetic phosphorylation Science 134 1425–1425

    Google Scholar 

  • ES Bamberger D King DL Erbes M Gibbs (1982) ArticleTitleH2 and CO2 evolution by anaerobically adapted Chlamydomonas reinhardtiiF-60 Plant Physiol 69 1268–1273

    Google Scholar 

  • F Berkovitch Y Nicolet JT Wan JT Jarrett CL Drennan (2004) ArticleTitleCrystal structure of biotin synthase, an S-adenosylmethionine-dependent radical enzyme Science. 303 76–79 Occurrence Handle10.1126/science.1088493 Occurrence Handle14704425

    Article  PubMed  Google Scholar 

  • M Bernhard T Buhrker B Bleijlevens AL Lacey ParticleDe VM Fernandes PJ Albracht B Friedrich (2001) ArticleTitleThe H2 sensor of Ralstonia eutropha J Biol Chem 76 15592–15597 Occurrence Handle10.1074/jbc.M009802200

    Article  Google Scholar 

  • VA Boichenko E Greenbaum M Seibert (2004) Hydrogen production by photosynthetic microorganisms MD Archer J Barber (Eds) Photoconversion of Solar Energy: Molecular to Global Photosynthesis, Vol 2, Imperial College Press London 397–452

    Google Scholar 

  • JJ Brand JN Wright S Lien (1989) ArticleTitleHydrogen production by eukaryotic algae Biotechnol Bioeng 33 1482–1488 Occurrence Handle10.1002/bit.260331116

    Article  Google Scholar 

  • HC Chen K Yokthongwattana AJ Newton A Melis (2003) ArticleTitle SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii Planta 218 98–106 Occurrence Handle12883888

    PubMed  Google Scholar 

  • D Dauvillée C Colleoni G Mouille A Buléon DJ Gallant B Bouchet MK Morell C d’Hulst AM Myers SG Ball (2001) ArticleTitleTwo loci control phytoglycogen produiction in the monocellular green alga Chlamydomonas reinhardtii Plant Physiol 125 1710–1722 Occurrence Handle10.1104/pp.125.4.1710 Occurrence Handle11299352

    Article  PubMed  Google Scholar 

  • L Florin A Tsokoglou T Happe (2001) ArticleTitleA novel type of [Fe]-hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain J Biol Chem 276 6125–6132 Occurrence Handle10.1074/jbc.M008470200 Occurrence Handle11096090

    Article  PubMed  Google Scholar 

  • T Flynn M Ghirardi M Seibert (2002) ArticleTitleAccumulation of O2-tolerant phenotypes in H2-producing strains of Chlamydomonas reinhardtii by sequential applications of chemical mutagenesis and selection Int J Hydrogen Energy 27 1421–1430 Occurrence Handle10.1016/S0360-3199(02)00117-9

    Article  Google Scholar 

  • M Forestier P King L Zhang M Posewitz S Schwarzer T Happe ML Ghirardi M Seibert (2003) ArticleTitleExpression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions Eur J Biochem 270 2750–2758 Occurrence Handle10.1046/j.1432-1033.2003.03656 Occurrence Handle12823545

    Article  PubMed  Google Scholar 

  • PA Frey (2001) ArticleTitleRadical mechanisms of enzymatic catalysis Annu Rev Biochem 70 121–148 Occurrence Handle10.1146/annurev.biochem.70.1.121 Occurrence Handle11395404

    Article  PubMed  Google Scholar 

  • H Gaffron (1939) ArticleTitleReduction of CO2 with H2 in green plants Nature 143 204–205

    Google Scholar 

  • H Gaffron (1940) ArticleTitleCarbon dioxide reduction with molecular hydrogen in green algae Am J Bot 27 273–283

    Google Scholar 

  • H Gaffron J Rubin (1942) ArticleTitleFermentative and photochemical production of hydrogen in algae J Gen Physiol 26 219–240 Occurrence Handle10.1085/jgp.26.2.219

    Article  Google Scholar 

  • ML Ghirardi RK Togasaki M Seibert (1997) ArticleTitleOxygen sensitivity of algal H2 production Appl Biochem Biotechnol 63–65 141–151

    Google Scholar 

  • ML Ghirardi L Zhang JW Lee T Flynn M Seibert E Greenbaum A Melis (2000) ArticleTitleMicroalgae: a green source of renewable H2 Trends Biotechnol 18 506–511 Occurrence Handle11102662

    PubMed  Google Scholar 

  • E Greenbaum (1982) ArticleTitlePhotosynthetic hydrogen and oxygen production: kinetic studies Science 196 879–880

    Google Scholar 

  • E Greenbaum (1988) ArticleTitleEnergetic efficiency of H2 photoevolution by algal water-splitting Biophys J 54 365–368

    Google Scholar 

  • T Happe A Kaminski (2002) ArticleTitleDifferential regulation of the [Fe]-hydrogenase during anaerobic adaptation in the gree alga Chlamydomonasreinhardtii Eur J Biochem 269 1022–1032 Occurrence Handle10.1046/j.0014-2956.2001.02743.x Occurrence Handle11846805

    Article  PubMed  Google Scholar 

  • T Happe JD Naber (1993) ArticleTitleIsolation, characterization and N-terminal amino acid sequence of hydrogenase from green alga Chlamydomonas reinhardtii Eur J Biochem 214 475–481 Occurrence Handle10.1111/j.1432-1033.1993.tb17944.x Occurrence Handle8513797

    Article  PubMed  Google Scholar 

  • T Happe B Mosler JD Naber (1994) ArticleTitleInduction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii Eur J Biochem 222 769–774 Occurrence Handle10.1111/j.1432-1033.1994.tb18923.x Occurrence Handle8026490

    Article  PubMed  Google Scholar 

  • T Happe M Winkler A Hemschemeier A Kaminski (2002) ArticleTitleHydrogenases in green algae: Do they save the algae’s life and solve our energy problems Trends Plant Sci 7 246–250 Occurrence Handle10.1016/S1360-1385(02)02274-4 Occurrence Handle12049920

    Article  PubMed  Google Scholar 

  • D Horner B Heil T Happe M Embley (2002) ArticleTitleIron hydrogenases, ancient enzymes in modern eukaryotes Trends Biochem Sci 27 148–153 Occurrence Handle10.1016/S0968-0004(01)02053-9 Occurrence Handle11893512

    Article  PubMed  Google Scholar 

  • E Kessler (1973) ArticleTitleEffect of anaerobiosis on photosynthetic reactions and nitrogen metabolism of algae with and without hydrogenase Arch Microbiol 93 91–100

    Google Scholar 

  • E Kessler (1974) Hydrogenase, photoreduction and anaerobic growth of algae WDP Stewart (Eds) Algal Physiology and Biochemistry Blackwell Oxford 456–473

    Google Scholar 

  • S Kosourov M Seibert ML Ghirardi (2003) ArticleTitleEffects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures Plant Cell Physiol 44 146–155 Occurrence Handle10.1093/pcp/pcg020 Occurrence Handle12610217

    Article  PubMed  Google Scholar 

  • S Kosourov A Tsygankov M Seibert ML Ghirardi (2002) ArticleTitleSustained hydrogen photoproduction by Chlamydomonas reinhardtii: effects of Culture parameters Biotechnol Bioeng 78 731–740 Occurrence Handle10.1002/bit.10254 Occurrence Handle12001165

    Article  PubMed  Google Scholar 

  • C Krebs TF Henshaw J Cheek BH Huynh JB Broderick (2000) ArticleTitleConversion of 3Fe–4S to 4Fe–4S clusters in native pyruvate formate-lyase activating enzyme: mössbauer characterization and implications for the mechanism J Am Chem Soc 122 12497–12506 Occurrence Handle10.1021/ja003335p

    Article  Google Scholar 

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

    Google Scholar 

  • S Lien Pietro S San (1981) ArticleTitleEffect of uncouplers on anaerobic adaptation of hydrogenase activity in C. reinhardtii. Biochem Biophys Res Commun 103 139–147 Occurrence Handle10.1016/0006-291X(81)91671-5 Occurrence Handle7032520

    Article  PubMed  Google Scholar 

  • A Melis T Happe (2001) ArticleTitleHydrogen production: green algae as a source of energy Plant Physiol 127 740–748 Occurrence Handle11706159

    PubMed  Google Scholar 

  • A Melis J Neidhardt JR Benemann (1999) ArticleTitle 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 Occurrence Handle10.1023/A:1008076231267

    Article  Google Scholar 

  • A Melis L Zhang M Forestier ML Ghirardi M Seibert (2000) ArticleTitleSustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii Plant Physiol 122 127–135 Occurrence Handle10631256

    PubMed  Google Scholar 

  • J Meyer J Gagnon (1991) ArticleTitlePrimary structure of hydrogenase I from Clostridium pasteurianum Biochem 30 9697–9704 Occurrence Handle10.1021/bi00104a018

    Article  Google Scholar 

  • K Miyamoto Y Nawa S Matsuoka S Ohta Y Miura (1990) ArticleTitleMechanism of adaptation and hydrogen photoproduction in a marine green alga, Chlamydomonas sp. MGA 161. J Ferment Bioengin 70 66–69 Occurrence Handle10.1016/0922-338X(90)90034-T

    Article  Google Scholar 

  • Y Montet P Amara A Volbeda X Vernede EC Hatchikian MJ Field M Frey JC Fontecilla-Camps (1997) ArticleTitleGas access to the active site of Ni–Fe hydrogenases probed by X-ray crystallography and molecular dynamics Nat Struct Biol 4 523–526 Occurrence Handle10.1038/nsb0797-523 Occurrence Handle9228943

    Article  PubMed  Google Scholar 

  • Nenoff TM (2000) Defect-free thin film membranes for H2 separation and isolation. Proceedings of the 2000 Hydrogen Program Review, NREL/CP-570–28890 (http://www.eere.energy.gov/hydrogenandfuelcells/pdfs/28890q.pdf)

  • Y Nicolet C Piras P Legrand CE Hatchikian JC Fontecilla-Camps (1998) ArticleTitle Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center Structure 7 13–23 Occurrence Handle10.1016/S0969-2126(99)80005-7

    Article  Google Scholar 

  • S Ollagnier-de-Choudens E Mulliez KS Hewitson M Fontecave (2002a) ArticleTitleBiotin synthase is a pyridoxal phosphate-dependent cysteine desulfurase Biochem 41 9145–9152 Occurrence Handle10.1021/bi0122011

    Article  Google Scholar 

  • S Ollagnier-de-Choudens Y Sanakis KS Hewitson P Roach E Munck M Fontecave (2002b) ArticleTitleReductive cleavage of S-adenosylmethionine by biotin synthase from Escherichia coli J Biol Chem 277 13449–13454 Occurrence Handle10.1074/jbc.M111324200

    Article  Google Scholar 

  • A Paschos RS Glass A Bock (2001) ArticleTitleCarbamoylphosphate requirements for synthesis of the active center of [NiFe]-hydrogenases FEBS Lett 488 9–12 Occurrence Handle10.1016/S0014-5793(00)02408-X Occurrence Handle11163786

    Article  PubMed  Google Scholar 

  • JW Peters WN Lanzilotta BJ Lemon LC Seefeldt (1998) ArticleTitleX-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom resolution Science 282 1853–1858 Occurrence Handle10.1126/science.282.5395.1853 Occurrence Handle9836629

    Article  PubMed  Google Scholar 

  • JEW Polle S Kanakagiri A Melis (2003) ArticleTitle tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size Planta 217 49–59 Occurrence Handle12721848

    PubMed  Google Scholar 

  • MC Posewitz PW King SL Smolinski L Zhang M Seibert ML Ghirardi (2004a) ArticleTitleDiscovery of two novel radical SAM proteins required for the assembly of an active [Fe]-hydrogenase J Biol Chem 279 25711–25720 Occurrence Handle10.1074/jbc.M403206200

    Article  Google Scholar 

  • MC Posewitz SL Smolinski S Kanakagiri A Melis M Seibert M Ghirardi (2004b) ArticleTitleHydrogen photoproduction is attenuated by disruption of an isoamylase gene in Chlamydomonas reinhardtii Plant Cell 16 2151–2163 Occurrence Handle10.1105/tpc.104.021972

    Article  Google Scholar 

  • S Reissmann E Hochleitner H Wang A Paschos F Lottspeich RS Glass A Bock (2003) ArticleTitleTaming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands Science 299 1067–1070 Occurrence Handle10.1126/science.1080972 Occurrence Handle12586941

    Article  PubMed  Google Scholar 

  • PG Roessler S Lein (1984) ArticleTitlePurification of hydrogenase from Chlamydomonas reinhardtii Plant Physiol 75 705–709

    Google Scholar 

  • R Schulz (1996) ArticleTitleHydrogenases and hydrogen production in eukaryotic organisms and cyanobacteria J Mar Biotechnol 4 16–22

    Google Scholar 

  • CD Silflow RL Chisholm TW Conner LP Ranum (1985) ArticleTitleThe two alpha-tubulin genes of Chlamydomonas reinhardtii code for slightly different proteins Mol Cell Biol 5 2389–2398 Occurrence Handle3855249

    PubMed  Google Scholar 

  • HJ Sofia G Chen BG Hetzler JF Reyes-Spindola NE Miller (2001) ArticleTitleRadical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods Nucleic Acids Res 29 1097–1106 Occurrence Handle10.1093/nar/29.5.1097 Occurrence Handle11222759

    Article  PubMed  Google Scholar 

  • M Stirnberg T Happe (2004) Identification of a cis-acting element controlling anaerobic expression of the HydA gene from Chlamydomonas reinhardtii. J Miyake Y Igarashi M Roegner (Eds) Biohydrogen III Elsevier Science Oxford

    Google Scholar 

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

    Google Scholar 

  • TS Stuart H Gaffron (1972b) ArticleTitleThe mechanism of hydrogen photoproduction by several algae. II. The contribution of photosystem II. Planta (Berlin) 106 101–112

    Google Scholar 

  • A Tomitani K Okada H Miyashita HCP Matthijs T Ohno A Tanaka (1999) ArticleTitleChlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts Nature 400 159–162 Occurrence Handle10.1038/22101 Occurrence Handle10408441

    Article  PubMed  Google Scholar 

  • NB Ugulava BR Gibney JT Jarrett (2000) ArticleTitleIron-sulfur cluster interconversions in biotin synthase: dissociation and reassociation of iron during conversion of [2Fe–2S] to [4Fe–4S] clusters Biochem. 39 5206–5214 Occurrence Handle10.1021/bi9926227

    Article  Google Scholar 

  • PM Vignais B Billoud J Meyer (2001) ArticleTitleClassification and phylogeny of hydrogenases FEMS Micro Rev 25 455–501 Occurrence Handle10.1016/S0168-6445(01)00063-8

    Article  Google Scholar 

  • A Volbeda Y Montet X Vernède EC Hatchikian JC Fontecilla-Camps (2002) ArticleTitleHigh-resolution crystallographic analysis of Desulfovibrio fructosovorans [NiFe] hydrogenase Int J Hydrogen Energy 27 1449–1461 Occurrence Handle10.1016/S0360-3199(02)00072-1

    Article  Google Scholar 

  • M Winkler B Heil B Hei T Happe (2002a) ArticleTitleIsolation and molecular characterization of the [Fe]-hydrogenase from the unicellular green alga Chlorella fusca Biochim Biophys Acta 1576 330–334

    Google Scholar 

  • M Winkler A Hemschemeier C Gotor A Melis T Happe (2002b) ArticleTitle[Fe]-hydrogenases in green algae: Photo-fermentation and hydrogen evolution under sulfur deprivation Int J Hydrogen Energy 27 1431–1439 Occurrence Handle10.1016/S0360-3199(02)00095-2

    Article  Google Scholar 

  • M Winkler C Maeurer A Hemschemeier T Happe (2004) The isolation of green algal strains with outstanding H2-productivity J Miyake Y Igarashi M Roegner (Eds) Biohydrogen III Elsevier Science Oxford

    Google Scholar 

  • R Wünschiers K Stangier H Senger R Schulz (2001) ArticleTitleMolecular evidence for an [Fe]-hydrogenase in the green alga Scenedesmus obliquus Curr Microbiol 42 353–360 Occurrence Handle10.1007/s002840010229 Occurrence Handle11400057

    Article  PubMed  Google Scholar 

  • DD Wykoff JP Davies A Melis AR Grossman (1998) ArticleTitleThe regulation of photosynthetic electron-transport during nutrient deprivation in Chlamydomonas reinhardtii Plant Physiol 117 129–139 Occurrence Handle9576782

    PubMed  Google Scholar 

  • L Zhang A Melis (2002) ArticleTitleProbing green algal hydrogen production Philos Trans R Soc Lond Biol Sci 357 1499–1509 Occurrence Handle10.1098/rstb.2002.1152

    Article  Google Scholar 

  • L Zhang T Happe A Melis (2002) ArticleTitleBiochemical and morphological characterization of sulfur deprived and H2-producing Chlamydomonas reinhardtii (green algae) Planta 214 552–561 Occurrence Handle11925039

    PubMed  Google Scholar 

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  1. Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA, 94720-3102, USA

    Anastasios Melis

  2. Basic Science Center, National Renewable Energy Laboratory, 1617 Cole Blvd, Golden, CO, 80401, USA

    Michael Seibert

  3. Lehrstuhl Biochemie der Pflanzen AG Photobiotechnologie, Ruhr Universität Bochum, 4630, Bochum, Germany

    Thomas Happe

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  1. Anastasios Melis
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Melis, A., Seibert, M. & Happe, T. Genomics of green algal hydrogen research. Photosynth Res 82, 277–288 (2004). https://doi.org/10.1007/s11120-004-2050-2

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