Abstract
The production of H2 for use as a renewable energy carrier using solar energy and electrons derived from water is widely regarded as one of the most environmentally benign and sustainable energy solutions. Several water-oxidizing, phototrophic algae and cyanobacteria have the remarkable ability to use low potential electrons from the photosynthetic electron transport chain, or from sugar oxidation, to reduce protons to H2. major research efforts are aimed at developing a more informed understanding of the physiological parameters dictating H2 production in water-oxidizing, phototrophic microorganisms, with the ultimate goal of improving H2 yields. Currently, the yields of H2 production are far below those required for the economically-viable production of H2 and substantial improvements are required to generate the quantities of H2 necessary to replace a meaningful portion of our current energy portfolio. Nevertheless, recent biological H2 production research efforts are rapidly elucidating (a) the metabolic pathways that supply reductant to H2-producing enzymes, (b) the metabolic and mechanistic requirements for maturation of the metallo-enzyme centers required in H2-producing enzymes, (c) novel hydrogenase enzymes, and (d) the genetic techniques required for manipulating metabolism in H2-producing organisms.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abed RM, Dobretsov S, Sudesh K (2009) Applications of cyanobacteria in biotechnology. J Appl Microbiol 106(1):1–12
Abeles FB (1964) Cell-free hydrogenase from Chlamydomonas. Plant Physiol 39:169–176
Adams MWW (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020(2):115–145
Ananyev G, Dismukes GC (2005) How fast can photosystem II split water? kinetic performance at high and low frequencies. Photosynth Res 84(1–3):355–365
Ananyev G, Carrieri D, Dismukes GC (2008) Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the cyanobacterium “Arthrospira (Spirulina) maxima”. Appl Environ Microbiol 74(19):6102–6113
Angermayr SA, Hellingwerf KJ, Lindblad P, de Mattos MJ (2009) Energy biotechnology with cyanobacteria. Curr Opin Biotechnol 20(3):257–263
Aparicio PJ, Azuara MP, Ballesteros A, Fernandez VM (1985) Effects of light-intensity and oxidized Nitrogen-sources on Hydrogen-production by Chlamydomonas-reinhardii. Plant Physiol 78(4):803–806
Appel J, Schulz R (1996) Sequence analysis of an operon of a NAD(P)-reducing nickel hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 gives additional evidence for direct coupling of the enzyme to NAD(P)H-dehydrogenase (complex I). Biochim Biophys Acta 1298(2):141–147
Appel J, Phunpruch S, Steinmuller K, Schulz R (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch Microbiol 173(5–6):333–338
Armstrong FA (2004) Hydrogenases: active site puzzles and progress. Curr Opin Chem Biol 8(2):133–140
Atanassova A, Zamble DB (2005) Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel. J Bacteriol 187(14):4689–4697
Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281(15):9909–9918
Bagley KA, Van Garderen CJ, Chen M, Duin EC, Albracht SP, Woodruff WH (1994) Infrared studies on the interaction of carbon monoxide with divalent nickel in hydrogenase from Chromatium vinosum. Biochemistry 33(31):9229–9236
Balk J, Pierik AJ, Netz DJ, Muhlenhoff U, Lill R (2004) The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J 23(10):2105–2115
Bamberger ES, King D, Erbes DL, Gibbs M (1982) H2 and CO2 evolution by anaerobically adapted Chlamydomonas reinhardtii F-60. Plant Physiol 69(6):1268–1273
Barney BM, Igarashi RY, Dos Santos PC, Dean DR, Seefeldt LC (2004) Substrate interaction at an iron-sulfur face of the FeMo-cofactor during nitrogenase catalysis. J Biol Chem 279(51):53621–53624
Barney BM, Laryukhin M, Igarashi RY, Lee HI, Dos Santos PC, Yang TC, Hoffman BM, Dean DR, Seefeldt LC (2005) Trapping a hydrazine reduction intermediate on the nitrogenase active site. Biochemistry 44(22):8030–8037
Barney B, Lee H, Santos P, Hoffman B, Dean D, Seefeldt L (2006) Breaking the N2 triple bond: insights into the nitrogenase mechanism. Dalton Trans 19:2277–2284
Barney BM, Lukoyanov D, Igarashi RY, Laryukhin M, Yang T-C, Dean DR, Hoffman BM, Seefeldt LC (2009) Trapping an intermediate of dinitrogen (N2) reduction on nitrogenase. Biochemistry 48(38):9094–9102
Beckmann J, Lehr F, Finazzi G, Hankamer B, Posten C, Wobbe L, Kruse O (2009) Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. J Biotechnol 142(1):70–77
Beer LL, Boyd ES, Peters JW, Posewitz MC (2009) Engineering algae for biohydrogen and biofuel production. Curr Opin Biotechnol 20(3):264–271
Ben-Amotz A, Gibbs M (1975) H2 metabolism in photosynthetic organisms II. Light-dependent H2 evolution by preparations from Chlamydomonas, Scenedesmus and spinach. Biochem Biophys Res Commun 64(1):355–359
Bennett B, Lemon BJ, Peters JW (2000) Reversible carbon monoxide binding and inhibition at the active site of the Fe-only hydrogenase. Biochemistry 39(25):7455–7460
Bennoun P (1998) Chlororespiration, sixteen years later. In: Rochaix JD, Goldschmiidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, pp 675–683
Bernard L, Desplats C, Mus F, Cuine S, Cournac L, Peltier G (2006) Agrobacterium tumefaciens type II NADH dehydrogenase. Characterization and interactions with bacterial and thylakoid membranes. FEBS J 273(15):3625–3637
Bernat G, Waschewski N, Rogner M (2009) Towards efficient hydrogen production: the impact of antenna size and external factors on electron transport dynamics in Synechocystis PCC 6803. Photosynth Res 99(3):205–216
Bhosale SH, Pant A, Khan MI (2009) Purification and characterization of putative alkaline [Ni-Fe] hydrogenase from unicellular marine green alga, Tetraselmis kochinensis NCIM 1605. Microbiol Res 164(2):131–137
Bishop PE, Joerger RD (2003) Genetics and molecular niology of alternative Nitrogen fixation systems. Annu Rev Plant Physiol Plant Mol Biol 41(1):109–125
Bishop PE, Jarlenski DM, Hetherington DR (1980) Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. Proc Natl Acad Sci USA 77(12):7342–7346
Bleijlevens B, Buhrke T, van der Linden E, Friedrich B, Albracht SP (2004) The auxiliary protein HypX provides oxygen tolerance to the soluble [NiFe]-hydrogenase of Ralstonia eutropha H16 by way of a cyanide ligand to nickel. J Biol Chem 279(45):46686–46691
Blokesch M, Bock A (2006) Properties of the [NiFe]-hydrogenase maturation protein HypD. FEBS Lett 580(17):4065–4068
Blokesch M, Paschos A, Theodoratou E, Bauer A, Hube M, Huth S, Bock A (2002) Metal insertion into NiFe-hydrogenases. Biochem Soc Trans 30(4):674–680
Blokesch M, Albracht SP, Matzanke BF, Drapal NM, Jacobi A, Bock A (2004a) The complex between hydrogenase-maturation proteins HypC and HypD is an intermediate in the supply of cyanide to the active site iron of [NiFe]-hydrogenases. J Mol Biol 344(1):155–167
Blokesch M, Paschos A, Bauer A, Reissmann S, Drapal N, Bock A (2004b) Analysis of the transcarbamoylation-dehydration reaction catalyzed by the hydrogenase maturation proteins HypF and HypE. Eur J Biochem 271(16):3428–3436
Bock A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71
Bohm R, Sauter M, Bock A (1990) Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol 4(2):231–243
Boichenko VA, Hoffmann P (1994) Photosynthetic hydrogen-production in prokaryotes and eukaryotes: occurrence, mechanism, and functions. Photosynthetica 30:527–552
Boichenko VA, Greenbaum E, Seibert M (2004) Hydrogen production by photosynthetic microorganisms. In: Archer MD, Barber J (eds) Photoconversion of solar energy, molecular to global photosynthesis, vol 2. Imperial College Press, London, pp 397–452
Boison G, Bothe H, Schmitz O (2000) Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR. Curr Microbiol 40(5):315–321
Bolling C, Fiehn O (2005) Metabolite profiling of Chlamydomonas reinhardtii under nutrient deprivation. Plant Physiol 139(4):1995–2005
Boyd ES, Spear JR, Peters JW (2009) [FeFe] hydrogenase genetic diversity provides insight into molecular adaptation in a saline microbial mat community. Appl Environ Microbiol 75(13):4620–4623
Brand JJ, Wright JN, Lien S (1989) Hydrogen-production by eukaryotic algae. Biotechnol Bioeng 33(11):1482–1488
Brazzolotto X, Rubach JK, Gaillard J, Gambarelli S, Atta M, Fontecave M (2006) The [Fe-Fe]-hydrogenase maturation protein HydF from Thermotoga maritima is a GTPase with an iron-sulfur cluster. J Biol Chem 281(2):769–774
Brigle KE, Weiss MC, Newton WE, Dean DR (1987) Products of the iron-molybdenum cofactor-specific biosynthetic genes, nifE and nifN, are structurally homologous to the products of the nitrogenase molybdenum-iron protein genes, nifD and nifK. J Bacteriol 169(4):1547–1553
Buhrke T, Lenz O, Krauss N, Friedrich B (2005) Oxygen tolerance of the H2-sensing [NiFe] hydrogenase from Ralstonia eutropha H16 is based on limited access of oxygen to the active site. J Biol Chem 280(25):23791–23796
Bulen WA, LeComte JR (1966) The nitrogenase system from Azotobacter: two-enzyme requirement for N2 reduction, ATP-dependent H2 evolution, and ATP hydrolysis. Proc Natl Acad Sci USA 56(3):979–986
Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B (2005) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10(2–4):181–196
Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96(7):2983–3012
Carrasco CD, Buettner JA, Golden JW (1995) Programmed DNA rearrangement of a cyanobacterial hupL gene in heterocysts. Proc Natl Acad Sci USA 92(3):791–795
Carrasco CD, Holliday SD, Hansel A, Lindblad P, Golden JW (2005) Heterocyst-specific excision of the Anabaena sp. strain PCC 7120 hupL element requires xisC. J Bacteriol 187(17):6031–6038
Cayol JL, Ollivier B, Patel BK, Prensier G, Guezennec J, Garcia JL (1994) Isolation and characterization of Halothermothrix orenii gen. nov., sp. nov., a halophilic, thermophilic, fermentative, strictly anaerobic bacterium. Int J Syst Bacteriol 44(3):534–540
Chan MK, Kim J, Rees DC (1993) The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 Å resolution structures. Science 260(5109):792–794
Chen C, Gibbs M (1992) Coupling of carbon-dioxide fixation to the oxyhydrogen reaction in the isolated chloroplast of Chlamydomonas reinhardtii. Plant Physiol 100(3):1361–1365
Chen HC, Melis A (2004) Localization and function of SulP, a nuclear-encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta 220(2):198–210
Chen Z, Lemon BJ, Huang S, Swartz DJ, Peters JW, Bagley KA (2002) Infrared studies of the CO-inhibited form of the Fe-only hydrogenase from Clostridium pasteurianum I: examination of its light sensitivity at cryogenic temperatures. Biochemistry 41(6):2036–2043
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(1):98–106
Chen HC, 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(1–3):289–296
Chivian D, Brodie EL et al (2008) Environmental genomics reveals a single-species ecosystem deep within Earth. Science 322(5899):275–278
Chochois V, Dauvillee D, Beyly A, Tolleter D, Cuine S, Timpano H, Ball S, Cournac L, Peltier G (2009) Hydrogen production in Chlamydomonas: photosystem II-dependent and -independent pathways differ in their requirement for starch metabolism. Plant Physiol 151(2):631–640
Christie PD, Lee H-I, Cameron LM, Hales BJ, Orme-Johnson WH, Hoffman BM (1996) Identification of the CO-binding cluster in nitrogenase MoFe protein by ENDOR of 57Fe isotopomers. J Am Chem Soc 118(36):8707–8709
Cinco RM, Macinnis JM, Greenbaum E (1993) The role of carbon-dioxide in light-activated hydrogen-production by Chlamydomonas reinhardtii. Photosynth Res 38(1):27–33
Cohen J, Kim K, King P, Seibert M, Schulten K (2005a) Finding gas diffusion pathways in proteins: application to O2 and H2 transport in CpI [FeFe]-hydrogenase and the role of packing defects. Structure 13(9):1321–1329
Cohen J, Kim K, Posewitz M, Ghirardi ML, Schulten K, Seibert M, King P (2005b) Molecular dynamics and experimental investigation of H2 and O2 diffusion in [Fe]-hydrogenase. Biochem Soc Trans 33(1):80–82
Colebatch G, Trevaskis B, Udvardi M (2002) Symbiotic nitrogen fixation research in the postgenomics era. New Phytol 153(1):37–42, (Repeated)
Corbett MC, Hu Y, Fay AW, Ribbe MW, Hedman B, Hodgson KO (2006) Structural insights into a protein-bound iron-molybdenum cofactor precursor. Proc Natl Acad Sci USA 103(5):1238–1243
Cournac L, Redding K, Ravenel J, Rumeau D, Josse EM, Kuntz M, Peltier G (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275(23):17256–17262
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(11–12):1229–1237
Cournac L, Guedeney G, Peltier G, Vignais PM (2004) Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. J Bacteriol 186(6):1737–1746
Cracknell JA, Wait AF, Lenz O, Friedrich B, Armstrong FA (2009) A kinetic and thermodynamic understanding of O2 tolerance in [NiFe]-hydrogenases. Proc Natl Acad Sci USA 106(49):20681–20686
Curatti L, Ludden PW, Rubio LM (2006) NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Proc Natl Acad Sci USA 103(14):5297–5301
Czech I, Silakov A, Lubitz W, Happe T (2009) The [FeFe]-hydrogenase maturase HydF from Clostridium acetobutylicum contains a CO and CN− ligated iron cofactor. FEBS Lett 584(3):638–642
Dance I (2003) The consequences of an interstitial N atom in the FeMo cofactor of nitrogenase. Chem Commun 2003(3):324–325
Davis LC, Henzl MT, Burris RH, Orme-Johnson WH (1979) Iron-sulfur clusters in the molybdenum-iron protein component of nitrogenase. Electron paramagnetic resonance of the carbon monoxide inhibited state. Biochemistry 18(22):4860–4869
de Lacey A, Fernandez V, Rousset M (2005) Native and mutant nickel-iron hydrogenases: unravelling structure and function. Coord Chem Rev 249(15–16):1596–1608
De Lacey AL, Fernandez VM, Rousset M, Cammack R (2007) Activation and inactivation of hydrogenase function and the catalytic cycle: spectroelectrochemical studies. Chem Rev 107(10):4304–4330
Deeth R, Field C (1994) A computational study of metal–dinitrogen co-ordination. J Chem Soc Dalton Trans 1994(13):1943–1948
DeLano WL (2002) The PyMol molecular graphics system at http://www.pymol.org
Dementin S, Leroux F, Cournac L, de Lacey AL, Volbeda A, Leger C, Burlat B, Martinez N, Champ S, Martin L, Sanganas O, Haumann M, Fernandez VM, Guigliarelli B, Fontecilla-Camps JC, Rousset M (2009) Introduction of methionines in the gas channel makes [NiFe] hydrogenase aero-tolerant. J Am Chem Soc 131(29):10156–10164
DemmigAdams B, Adams WW (1996) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198(3):460–470
Desplats C, Mus F, Cuine S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J Biol Chem 284(7):4148–4157
Doebbe A, Rupprecht J, Beckmann J, Mussgnug JH, Hallmann A, Hankamer B, Kruse O (2007) Functional integration of the HUP1 hexose symporter gene into the genome of C. reinhardtii: Impacts on biological H2 production. J Biotechnol 131(1):27–33
Dos Santos PC, Dean DR, Hu Y, Ribbe MW (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem Rev 104(2):1159–1173
Dos Santos PC, Igarashi RY, Lee H-I, Hoffman BM, Seefeldt LC, Dean DR (2005) Substrate interactions with the nitrogenase active site. Acc Chem Res 38(3):208–214
Driesener RC, Challand MR, McGlynn SE, Shepard EM, Boyd ES, Broderick JB, Peters JW, Roach PL (2010) [FeFe]-Hydrogenase cyanide ligands derived from S-adenosylmethionine-dependent cleavage of tyrosine. Angew Chem Int Ed Engl 49(9):1687–1690
Du Z, Li H, Gu T (2007) A state of the art review on microbial fuel cells: a promising technology for wastewater treatment and bioenergy. Biotechnol adv 25(5):464–482
Dubini A, Sargent F (2003) Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett 549(1–3):141–146
Dubini A, Mus F, Seibert M, Grossman AR, Posewitz MC (2009) Flexibility in anaerobic metabolism as revealed in a mutant of Chlamydomonas reinhardtii lacking hydrogenase activity. J Biol Chem 284(11):7201–7213
Duche O, Elsen S, Cournac L, Colbeau A (2005) Enlarging the gas access channel to the active site renders the regulatory hydrogenase HupUV of Rhodobacter capsulatus O2 sensitive without affecting its transductory activity. FEBS J 272(15):3899–3908
Dyall SD, Yan W, Delgadillo-Correa MG, Lunceford A, Loo JA, Clarke CF, Johnson PJ (2004) Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431(7012):1103–1107
Eady RR (1996) Structure–function relationships of alternative nitrogenases. Chem Rev 96(7):3013–3030
Einsle O, Tezcan FA, Andrade SL, Schmid B, Yoshida M, Howard JB, Rees DC (2002) Nitrogenase MoFe-protein at 1.16 A resolution: a central ligand in the FeMo-cofactor. Science 297(5587):1696–1700
Erbes D, King D, Gibbs M (1978) Effect of carbon-monoxide and oxygen on hydrogen activation by hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 61(4):23–23
Erbes D, King D, Gibbs M (1979) Inactivation of hydrogenase in cell-free-extracts and whole cells of Chlamydomonas reinhardtii by oxygen. Plant Physiol 63(6):1138–1142
Escoubas JM, Lomas M, LaRoche J, Falkowski PG (1995) Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. Proc Natl Acad Sci USA 92(22):10237–10241
Fan HJ, Hall MB (2001) A capable bridging ligand for Fe-only hydrogenase: density functional calculations of a low-energy route for heterolytic cleavage and formation of dihydrogen. J Am Chem Soc 123(16):3828–3829
Fan HJ, Hall MB (2002) High-spin Ni(II), a surprisingly good structural model for [NiFe] hydrogenase. J Am Chem Soc 124(3):394–395
Fani R, Gallo R, Lio P (2000) Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. J Mol Evol 51(1):1–11
Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Mol Biol Rev 56(2):340
Fedorov A, Kosourov S, Ghirardi M, Seibert M (2005) Continuous hydrogen photoproduction by Chlamydomonas reinhardtii. Appl Biochem Biotechnol 121:403–412
Fernandez V, Hatchikian E, Cammack R (1985) Properties and reactivation of two different deactivated forms of Desulfovibrio gigas hydrogenase. Biochim Biophys Acta 832:69–79
Fichtner C, Laurich C, Bothe E, Lubitz W (2006) Spectroelectrochemical characterization of the [NiFe] hydrogenase of Desulfovibrio vulgaris Miyazaki F. Biochemistry 45(32):9706–9716
Florin L, Tsokoglou A, Happe T (2001) A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain. J Biol Chem 276(9):6125–6132
Foerster S, Stein M, Brecht M, Ogata H, Higuchi Y, Lubitz W (2003) Single crystal EPR studies of the reduced active site of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J Am Chem Soc 125(1):83–93
Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107(10):4273–4303
Forestier M, King P, Zhang L, 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(13):2750–2758
Forzi L, Hellwig P, Thauer RK, Sawers RG (2007) The CO and CN− ligands to the active site Fe in [NiFe]-hydrogenase of Escherichia coli have different metabolic origins. FEBS Lett 581(17):3317–3321
Frazzon J, Dean DR (2003) Formation of iron-sulfur clusters in bacteria: an emerging field in bioinorganic chemistry. Curr Opin Chem Biol 7(2):166–173
Frazzon J, Fick JR, Dean DR (2002) Biosynthesis of iron-sulphur clusters is a complex and highly conserved process. Biochem Soc Trans 30(4):680–685
Frey PA, Hegeman AD, Ruzicka FJ (2008) The radical SAM superfamily. Crit Rev Biochem Mol Biol 43(1):63–88
Gaffron H (1942) Reduction of carbon dioxide coupledwith the oxyhydrogen reaction in algae. J Gen Physiol 26:241–267
Gaffron H (1944) Photosynthesis, photoreduction, and dark reduction of carbon dioxide in certain algae. Biol Rev 19:1–20
Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol 26:219–240
Garcin E, Vernede X, Hatchikian EC, Volbeda A, Frey M, Fontecilla-Camps JC (1999) The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Structure 7(5):557–566
George SJ, Igarashi RY, Piamonteze C, Soboh B, Cramer SP, Rubio LM (2007) Identification of a Mo-Fe-S cluster on NifEN by Mo K-edge extended X-ray absorption fine structure. J Am Chem Soc 129(11):3060–3061
George SJ, Igarashi RY, Xiao Y, Hernandez JA, Demuez M, Zhao D, Yoda Y, Ludden PW, Rubio LM, Cramer SP (2008) Extended X-ray absorption fine structure and nuclear resonance vibrational spectroscopy reveal that NifB-co, a FeMo-co precursor, comprises a 6Fe core with an interstitial light atom. J Am Chem Soc 130(17):5673–5680
Georgiadis MM, Komiya H, Chakrabarti P, Woo D, Kornuc JJ, Rees DC (1992) Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science 257(5077):1653–1659
Gfeller RP, Gibbs M (1984) Fermentative metabolism of Chlamydomonas reinhardtii, I: analysis of fermentative products from starch in dark and light. Plant Physiol 75:212–218
Ghirardi ML, Togasaki RK, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotechnol 63:141–151
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(12):506–511
Ghirardi ML, King PW, Posewitz MC, Maness PC, Fedorov A, Kim K, Cohen J, Schulten K, Seibert M (2005) Approaches to developing biological H2-photoproducing organisms and processes. Biochem Soc Trans 33(1):70–72
Ghirardi ML, Posewitz MC, Maness PC, Dubini A, Yu J, Seibert M (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu Rev Plant Biol 58:71–91
Ghirardi ML, Dubini A, Yu J, Maness PC (2009) Photobiological hydrogen-producing systems. Chem Soc Rev 38(1):52–61
Gibbs M, Gfeller RP, Chen C (1986) Fermentative metabolism of Chlamydomonas reinhardii: III. Photoassimilation of acetate. Plant Physiol 82(1):160–166
Gloaguen F, Rauchfuss TB (2009) Small molecule mimics of hydrogenases: hydrides and redox. Chem Soc Rev 38(1):100–108
Godde D, Trebst A (1980) NADH as electron-donor for the photosynthetic membrane of Chlamydomonas reinhardtii. Arch Microbiol 127(3):245–252
Goldet G, Wait AF, Cracknell JA, Vincent KA, Ludwig M, Lenz O, Friedrich B, Armstrong FA (2008) Hydrogen production under aerobic conditions by membrane-bound hydrogenases from Ralstonia species. J Am Chem Soc 130(33):11106–11113
Goodwin PJ, Agar JN, Roll JT, Roberts GP, Johnson MK, Dean DR (1998) The Azotobacter vinelandii NifEN complex contains two identical [4Fe-4S] clusters. Biochemistry 37(29):10420–10428
Gu W, Jacquamet L, Patil DS, Wang HX, Evans DJ, Smith MC, Millar M, Koch S, Eichhorn DM, Latimer M, Cramer SP (2003) Refinement of the nickel site structure in Desulfovibrio gigas hydrogenase using range-extended EXAFS spectroscopy. J Inorg Biochem 93(1–2):41–51
Hadfield KL, Bulen WA (1969) Adenosine triphosphate requirement of nitrogenase from Azotobacter vinelandii. Biochemistry 8(12):5103–5108
Hallenbeck PC (2009) Fermentative hydrogen production: principles, progress, and prognosis. Int J Hydrogen Energy 34(17):7379–7389
Hankamer B, Lehr F, Rupprecht J, Mussgnug JH, Posten C, Kruse O (2007) Photosynthetic biomass and H2 production by green algae: from bioengineering to bioreactor scale-up. Physiol Plant 131(1):10–21
Hansel A, Lindblad P (1998) Towards optimization of cyanobacteria as biotechnologically relevant producers of molecular hydrogen, a clean and renewable energy source. Appl Microbiol Biotechnol 50(2):153–160
Happe T, Kaminski A (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269(3):1022–1032
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(2):475–481
Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. Eur J Biochem 222(3):769–774
Happe RP, Roseboom W, Pierik AJ, Albracht SP, Bagley KA (1997) Biological activation of hydrogen. Nature 385(6612):126
Happe T, Schutz K, Bohme H (2000) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182(6):1624–1631
Happe T, Hemschemeier A, Winkler M, Kaminski A (2002) Hydrogenases in green algae: do they save the algae’s life and solve our energy problems? Trends Plant Sci 7(6):246–250
Haselkorn R, Buikema W (1992) Nitrogen fixation in cyanobacteria. In: Stacey GS, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 166–190
Hawkes FR, Dinsdale R, Hawkes DL, Hussy I (2002) Sustainable fermentative hydrogen production: challenges for process optimisation. Int J Hydrogen Energy 27(11–12):1339–1347
He SH, Teixeira M, LeGall J, Patil DS, Moura I, Moura JJ, DerVartanian DV, Huynh BH, Peck HD Jr (1989) EPR studies with 77Se-enriched (NiFeSe) hydrogenase of Desulfovibrio baculatus. Evidence for a selenium ligand to the active site nickel. J Biol Chem 264(5):2678–2682
Healey F (1970) Hydrogen evolution by several algae. Planta 91(3):220–226
Hedderich R, Forzi L (2005) Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10(2–4):92–104
Heidelberg JF, Paulsen IT et al (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol 20(11):1118–1123
Hemschemeier A, Happe T (2005) The exceptional photofermentative hydrogen metabolism of the green alga Chlamydomonas reinhardtii. Biochem Soc Trans 33(1):39–41
Hemschemeier A, Fouchard S, Cournac L, Peltier G, Happe T (2008) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 227(2):397–407
Hernandez JA, Igarashi RY, Soboh B, Curatti L, Dean DR, Ludden PW, Rubio LM (2007) NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway. Mol Microbiol 63(1):177–192
Higuchi Y, Yagi T, Yasuoka N (1997) Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 5(12):1671–1680
Higuchi Y, Ogata H, Miki K, Yasuoka N, Yagi T (1999) Removal of the bridging ligand atom at the Ni-Fe active site of [NiFe] hydrogenase upon reduction with H2, as revealed by X-ray structure analysis at 1.4 A resolution. Structure 7(5):549–556
Hoffman BM, Dean DR, Seefeldt LC (2009) Climbing nitrogenase: toward a mechanism of enzymatic nitrogen fixation. Acc Chem Res 42(5):609–619
Holland PL (2008) Electronic structure and reactivity of three-coordinate iron complexes. Acc Chem Res 41(8):905–914
Homann P (2003) Hydrogen metabolism of green algae: discovery and early research – a tribute to Hans Gaffron and his coworkers. Photosynth Res 76(1–3):93–103
Hoover TR, Robertson AD, Cerny RL, Hayes RN, Imperial J, Shah VK, Ludden PW (1987) Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate. Nature 329(6142):855–857
Hoover TR, Imperial J, Ludden PW, Shah VK (1988) Homocitrate cures the NifV- phenotype in Klebsiella pneumoniae. J Bacteriol 170(4):1978–1979
Houchins JP, Hind G (1984) Concentration and function of membrane-bound cytochromes in cyanobacterial heterocysts. Plant Physiol 76(2):456–460
Howard JB, Rees DC (1994) Nitrogenase: a nucleotide-dependent molecular switch. Annu Rev Biochem 63:235–264
Howard JB, Rees DC (2006) How many metals does it take to fix N2? a mechanistic overview of biological nitrogen fixation. Proc Natl Acad Sci USA 103(46):17088–17093
Hu Y, Fay AW, Ribbe MW (2005) Identification of a nitrogenase FeMo cofactor precursor on NifEN complex. Proc Natl Acad Sci USA 102(9):3236–3241
Hu Y, Corbett MC, Fay AW, Webber JA, Hodgson KO, Hedman B, Ribbe MW (2006) FeMo cofactor maturation on NifEN. Proc Natl Acad Sci USA 103(46):17119–17124
Hu Y, Fay AW, Lee CC, Yoshizawa J, Ribbe MW (2008) Assembly of nitrogenase MoFe protein. Biochemistry 47(13):3973–3981
Huyett JE, Carepo M, Pamplona A, Franco R, Moura I, Moura JJG, Hoffman BM (1997) 57Fe Q-band pulsed ENDOR of the hetero-dinuclear site of nickel hydrogenase: comparison of the NiA, NiB, and NiC states. J Am Chem Soc 119(39):9291–9292
Hwang JC, Chen CH, Burris RH (1973) Inhibition of nitrogenase-catalyzed reductions. Biochim Biophys Acta 292(1):256–270
Ihara M, Nishihara H, Yoon KS, Lenz O, Friedrich B, Nakamoto H, Kojima K, Honma D, Kamachi T, Okura I (2006) Light-driven hydrogen production by a hybrid complex of a [NiFe]-hydrogenase and the cyanobacterial photosystem I. Photochem Photobiol 82(3):676–682
Jackson DD, Ellms JW (1896) On odors and tastes of surface waters with special reference to Anabaena, a microscopical organism found in certain water supplies of Massachusetts. Rep Mass State Board Health 1896:410–420
Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583(2):325–329
Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuine S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci USA 105(51):20546–20551
Johnson DC, Dean DR, Smith AD, Johnson MK (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74(1):247–281
Kalia VC, Joshi AP (1995) Conversion of waste biomass (Pea-shells) into hydrogen and methane through anaerobic-digestion. Bioresour Technol 53(2):165–168
Kalia VC, Jain SR, Kumar A, Joshi AP (1994) Frementation of biowaste to H2 by Bacillus licheniformis. World J Microbiol Biotechnol 10(2):224–227
Kellers P, Ogata H, Lubitz W (2008) Purification, crystallization and preliminary X-ray analysis of the membrane-bound [NiFe] hydrogenase from Allochromatium vinosum. Acta Crystallogr Sect F Struct Biol Cryst Commun 64(Pt 8):719–722
Kessler E (1974) Hydrogenase, photoreduction and anaerobic growth. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell, Oxford, pp 456–473
Kim J, Rees DC (1992a) Structural models for the metal centers in the nitrogenase molybdenum-iron protein. Science 257(5077):1677–1682
Kim JS, Rees DC (1992b) Crystallographic structure and functional implications of the nitrogenase molybdenum–iron protein from Azotobacter vinelandii. Nature 360(6404):553–560
Kim CH, Newton WE, Dean DR (1995) Role of the MoFe protein alpha-subunit histidine-195 residue in FeMo-cofactor binding and nitrogenase catalysis. Biochemistry 34(9):2798–2808
Kim JK, Nhat L, Chun YN, Kim SW (2008) Hydrogen production conditions from food waste by dark fermentation with Clostridium beijerinckii KCTC 1785. Biotechnol Bioprocess Eng 13(4):499–504
King PW, Posewitz MC, Ghirardi ML, Seibert M (2006a) Functional studies of [FeFe] hydrogenase maturation in an Escherichia coli biosynthetic system. J Bacteriol 188(6):2163–2172
King PW, Svedruzic D, Cohen J, Schulten K, Seibert M, Ghirardi ML (2006b) Structural and functional investigations of biological catalysts for optimization of solar-driven, H2 production systems. In: Proceedings of the International Society for Optical Engineering, Solar Hydrogen and Nanotechnology, San Diego
Kleihues L, Lenz O, Bernhard M, Buhrke T, Friedrich B (2000) The H2 sensor of Ralstonia eutropha is a member of the subclass of regulatory [NiFe] hydrogenases. J Bacteriol 182(10):2716–2724
Kosourov SN, Seibert M (2009) Hydrogen photoproduction by nutrient-deprived Chlamydomonas reinhardtii cells immobilized within thin alginate films under aerobic and anaerobic conditions. Biotechnol Bioeng 102(1):50–58
Kovacs KL, Kovacs AT, Maroti G, Meszaros LS, Balogh J, Latinovics D, Fulop A, David R, Doroghazi E, Rakhely G (2005) The hydrogenases of Thiocapsa roseopersicina. Biochem Soc Trans 33:61–63
Kreuzberg K (1984) Starch fermentation via formate producing pathway in Chlamydomonas reinhardtii, Chlorogonium elongatum and Chlorella fusca. Physiol Plant 61(1):87–94
Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005a) Improved photobiological H2 production in engineered green algal cells. J Biol Chem 280(40):34170–34177
Kruse O, Rupprecht J, Mussgnug J, Dismukes G, Hankamer B (2005b) Photosynthesis: a blueprint for solar energy capture and biohydrogen production technologies. Photochem Photobiol Sci 4(12):957–970
Lamle SE, Albracht SP, Armstrong FA (2004) Electrochemical potential-step investigations of the aerobic interconversions of [NiFe]-hydrogenase from Allochromatium vinosum: insights into the puzzling difference between unready and ready oxidized inactive states. J Am Chem Soc 126(45):14899–14909
Lanyi JK (1974) Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol Rev 38(3):272–290
Laplaza CE, Cummins CC (1995) Dinitrogen cleavage by a three-coordinate Molybdenum(III) complex. Science 268(5212):861–863
Laurinavichene T, Tolstygina I, Tsygankov A (2004) The effect of light intensity on hydrogen production by sulfur-deprived Chlamydomonas reinhardtii. J Biotechnol 114(1–2):143–151
Laurinavichene TV, Kosourov SN, Ghirardi ML, Seibert M, Tsygankov AA (2008) Prolongation of H2 photoproduction by immobilized, sulfur-limited Chlamydomonas reinhardtii cultures. J Biotechnol 134(3–4):275–277
Leach MR, Zamble DB (2007) Metallocenter assembly of the hydrogenase enzymes. Curr Opin Chem Biol 11(2):159–165
Lee JW, Greenbaum E (2003) A new oxygen sensitivity and its potential application in photosynthetic H2 production. Appl Biochem Biotechnol 105:303–313
Lee S, Holm R (2004) The clusters of nitrogenase: synthetic methodology in the construction of weak-field clusters. Chem Rev 104(2):1135–1158
Lee H-I, Cameron LM, Hales BJ, Hoffman BM (1997) CO binding to the FeMo cofactor of CO-inhibited nitrogenase: 13CO and 1H Q-band ENDOR investigation. J Am Chem Soc 119(42):10121–10126
Lee H-I, Sorlie M, Christiansen J, Song R, Dean DR, Hales BJ, Hoffman BM (2000) Characterization of an intermediate in the reduction of acetylene by the nitrogenase α-Gln195 MoFe protein by Q-band EPR and 13C,1H ENDOR. J Am Chem Soc 122(23):5582–5587
Lee JW, Mets L, Greenbaum E (2002) Improvement of photosynthetic CO2 fixation at high light intensity through reduction of chlorophyll antenna size. Appl Biochem Biotechnol 98:37–48
Lee HI, Igarashi RY, Laryukhin M, Doan PE, Dos Santos PC, Dean DR, Seefeldt LC, Hoffman BM (2004) An organometallic intermediate during alkyne reduction by nitrogenase. J Am Chem Soc 126(31):9563–9569
Lee HI, Sorlie M, Christiansen J, Yang TC, Shao J, Dean DR, Hales BJ, Hoffman BM (2005) Electron inventory, kinetic assignment (E n ), structure, and bonding of nitrogenase turnover intermediates with C2H2 and CO. J Am Chem Soc 127(45):15880–15890
Lee CC, Blank MA, Fay AW, Yoshizawa JM, Hu Y, Hodgson KO, Hedman B, Ribbe MW (2009) Stepwise formation of P-cluster in nitrogenase MoFe protein. Proc Natl Acad Sci USA 106(44):18474–18478
Lemon BJ, Peters JW (1999) Binding of exogenously added carbon monoxide at the active site of the iron-only hydrogenase (CpI) from Clostridium pasteurianum. Biochemistry 38(40):12969–12973
Lemon BJ, Peters JW (2000) Photochemistry at the active site of the carbon monoxide inhibited form of the iron-only hydrogenase (CpI). J Am Chem Soc 122(15):3793–3794
Lenz O, Gleiche A, Strack A, Friedrich B (2005) Requirements for heterologous production of a complex metalloenzyme: the membrane-bound [NiFe] hydrogenase. J Bacteriol 187(18):6590–6595
Lenz O, Zebger I, Hamann J, Hildebrandt P, Friedrich B (2007) Carbamoylphosphate serves as the source of CN−, but not of the intrinsic CO in the active site of the regulatory [NiFe]-hydrogenase from Ralstonia eutropha. FEBS Lett 581(17):3322–3326
Leroux F, Dementin S, Burlat B, Cournac L, Volbeda A, Champ S, Martin L, Guigliarelli B, Bertrand P, Fontecilla-Camps J, Rousset M, Leger C (2008) Experimental approaches to kinetics of gas diffusion in hydrogenase. Proc Natl Acad Sci USA 105(32):11188–11193
Liebgott PP, Leroux F, Burlat B, Dementin S, Baffert C, Lautier T, Fourmond V, Ceccaldi P, Cavazza C, Meynial-Salles I, Soucaille P, Fontecilla-Camps JC, Guigliarelli B, Bertrand P, Rousset M, Leger C (2010) Relating diffusion along the substrate tunnel and oxygen sensitivity in hydrogenase. Nat Chem Biol 6(1):63–70
Lien S, Pietro AS (1981) Effect of uncouplers on anaerobic adaptation of hydrogenase activity in C reinhardtii. Biochem Biophys Res Commun 103(1):139–147
Lindberg P, Schütz K, Happe T, Lindblad P (2002) A hydrogen-producing, hydrogenase-free mutant strain of Nostoc punctiforme ATCC 29133. Int J Hydrogen Energy 27(11–12):1291–1296
Lindblad P, Christensson K, Lindberg P, Fedorov A, Pinto F, Tsygankov A (2002) Photoproduction of H2 by wildtype Anabaena PCC 7120 and a hydrogen uptake deficient mutant: from laboratory experiments to outdoor culture. Int J Hydrogen Energy 27(11–12):1271–1281
Liu Z, Hu P (2002) Mechanism of H2 metabolism on Fe-only hydrogenases. J Chem Phys 117(18):8177–8180
Liu H, Ramnarayanan R, Logan B (2004) Production of electricity during wastewater treatment using a single chamber microbial fuel cell. Environ Sci Technol 38(7):2281–2285
Liu H, Grot S, Logan B (2005) Electrochemically assisted microbial production of hydrogen from acetate. Environ Sci Technol 39(11):4317–4320
Logan B (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381
Logan B, Liu H (2004) Electricity generation using an air-cathode single chamber microbial fuel cell in the presence and absence of a proton exchange membrane. Environ Sci Technol 38(14):4040–4046
Lowe DJ, Thorneley RN (1984) The mechanism of Klebsiella pneumoniae nitrogenase action. The determination of rate constants required for the simulation of the kinetics of N2 reduction and H2 evolution. Biochem J 224(3):895–901
Lubner CE, Grimme R, Bryant DA, Golbeck JH (2010) Wiring photosystem I for direct solar hydrogen production. Biochemistry 49(3):404–414
Ludwig M, Schulz-Friedrich R, Appel J (2006) Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: implications for the phylogenetic origin of cyanobacterial and algal hydrogenases. J Mol Evol 63(6):758–768
Ma K, Weiss R, Adams MW (2000) Characterization of hydrogenase II from the hyperthermophilic archaeon Pyrococcus furiosus and assessment of its role in sulfur reduction. J Bacteriol 182(7):1864–1871
Magnuson A, Anderlund M, Johansson O, Lindblad P, Lomoth R, Polivka T, Ott S, Stensjo K, Styring S, Sundstrom V, Hammarstrom L (2009) Biomimetic and microbial approaches to solar fuel generation. Acc Chem Res 42(12):1899–1909
Maier T, Bock A (1996) Generation of active [NiFe] hydrogenase in vitro from a nickel-free precursor form. Biochemistry 35(31):10089–10093
Maier T, Jacobi A, Sauter M, Bock A (1993) The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J Bacteriol 175(3):630–635
Maier T, Lottspeich F, Bock A (1995) GTP hydrolysis by HypB is essential for nickel insertion into hydrogenases of Escherichia coli. Eur J Biochem 230(1):133–138
Maione T, Gibbs M (1986a) Hydrogenase-mediated activities in isolated chloroplasts of Chlamydomonas reinhardtii. Plant Physiol 80(2):360–363
Maione T, Gibbs M (1986b) Association of the chloroplastic repiratory and photosynthetic electron transport chains of Chlamydomonas reinhardtii with photoreduction and the oxyhydrogen reaction. Plant Physiol 80(2):364–368
Makarova VV, Kosourov S, Krendeleva TE, Semin BK, Kukarskikh GP, Rubin AB, Sayre RT, Ghirardi ML, Seibert M (2007) Photoproduction of hydrogen by sulfur-deprived C. reinhardtii mutants with impaired photosystem II photochemical activity. Photosynth Res 94(1):79–89
Maness PC, Smolinski S, Dillon AC, Heben MJ, Weaver PF (2002) Characterization of the oxygen tolerance of a hydrogenase linked to a carbon monoxide oxidation pathway in Rubrivivax gelatinosus. Appl Environ Microbiol 68(6):2633–2636
Maroti G, Tong YK, Yooseph S, Baden-Tillson H, Smith HO, Kovacs KL, Frazier M, Venter JC, Xu Q (2009) Discovery of [NiFe] hydrogenase genes in metagenomic DNA: cloning and heterologous expression in Thiocapsa roseopersicina. Appl Environ Microbiol 75(18):5821–5830
Marques MC, Coelho R, De Lacey AL, Pereira IA, Matias PM (2009) The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris hildenborough: a hydrogenase without a bridging ligand in the active aite in its oxidised, “as-isolated” state. J Mol Biol 396:893–907
Masepohl B, Schneider K, Drepper T, Müller A, Klipp W (2002) Alternative nitrogenases. In: Leigh GH (ed) Nitrogen fixation at the millennium. Elsevier Science, Amsterdam, pp 191–222
Masukawa H, Mochimaru M, Sakurai H (2002a) Disruption of the uptake hydrogenase gene, but not of the bidirectional hydrogenase gene, leads to enhanced photobiological hydrogen production by the nitrogen-fixing cyanobacterium Anabaena sp. PCC 7120. Appl Microbiol Biotechnol 58(5):618–624
Masukawa H, Mochimaru M, Sakurai H (2002b) Effects of disruption of hydrogenase genes in Anabaena sp. PCC 7120 on photobiological H2 production and nitrogenase activities. Plant Cell Physiol 43:S176–S176
Matias PM, Soares CM, Saraiva LM, Coelho R, Morais J, Le Gall J, Carrondo MA (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 A and modelling studies of its interaction with the tetrahaem cytochrome c3. J Biol Inorg Chem 6(1):63–81
Matthew T, Zhou W, Rupprecht J, Lim L, Thomas-Hall SR, Doebbe A, Kruse O, Hankamer B, Marx UC, Smith SM, Schenk PM (2009) The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion. J Biol Chem 284(35):23415–23425
May P, Wienkoop S, Kempa S, Usadel B, Christian N, Rupprecht J, Weiss J, Recuenco-Munoz L, Ebenhoh O, Weckwerth W, Walther D (2008) Metabolomics- and proteomics-assisted genome annotation and analysis of the draft metabolic network of Chlamydomonas reinhardtii. Genetics 179(1):157–166
Mayer SM, Lawson DM, Gormal CA, Roe SM, Smith BE (1999) New insights into structure-function relationships in nitrogenase: a 1.6 A resolution X-ray crystallographic study of Klebsiella pneumoniae MoFe-protein. J Mol Biol 292(4):871–891
Mayer S, Niehaus W, Dean D (2002) Reduction of short chain alkynes by a nitrogenase-70 Ala-substituted MoFe protein. J Chem Soc Dalton Trans 2002(5):802–807
McGlynn SE, Ruebush SS, Naumov A, Nagy LE, Dubini A, King PW, Broderick JB, Posewitz MC, Peters JW (2007) In vitro activation of [FeFe] hydrogenase: new insights into hydrogenase maturation. J Biol Inorg Chem 12(4):443–447
McGlynn SE, Shepard EM, Winslow MA, Naumov AV, Duschene KS, Posewitz MC, Broderick WE, Broderick JB, Peters JW (2008) HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis. FEBS Lett 582(15):2183–2187
Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177(4):272–280
Melis A, Happe T (2004) Trails of green alga hydrogen research – from Hans Gaffron to new frontiers. Photosynth Res 80(1–3):401–409
Melis A, Melnicki M (2006) Integrated biological hydrogen production. Int J Hydrogen Energy 31(11):1563–1573
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(1):127–136
Menon AL, Robson RL (1994) In vivo and in vitro nickel-dependent processing of the [NiFe] hydrogenase in Azotobacter vinelandii. J Bacteriol 176(2):291–295
Menon NK, Robbins J, Der Vartanian M, Patil D, Peck HD Jr, Menon AL, Robson RL, Przybyla AE (1993) Carboxy-terminal processing of the large subunit of [NiFe] hydrogenases. FEBS Lett 331(1–2):91–95
Meuser JE, Ananyev G, Wittig LE, Kosourov S, Ghirardi ML, Seibert M, Dismukes GC, Posewitz MC (2009) Phenotypic diversity of hydrogen production in chlorophycean algae reflects distinct anaerobic metabolisms. J Biotechnol 142(1):21–30
Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64(9):1063–1084
Montet Y, Amara P, Volbeda A, Vernede X, Hatchikian EC, Field MJ, Frey M, Fontecilla-Camps JC (1997) Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nat Struct Biol 4(7):523–526
Mulder DW, Ortillo DO, Gardenghi DJ, Naumov AV, Ruebush SS, Szilagyi RK, Huynh B, Broderick JB, Peters JW (2009) Activation of HydAΔEFG requires a preformed [4Fe-4S] cluster. Biochemistry 48(26):6240–6248
Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H2 photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708(3):322–332
Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282(35):25475–25486
Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5(6):802–814
Nagy LE, Meuser JE, Plummer S, Seibert M, Ghirardi ML, King PW, Ahmann D, Posewitz MC (2007) Application of gene-shuffling for the rapid generation of novel [FeFe]-hydrogenase libraries. Biotechnol Lett 29(3):421–430
Nakajima Y, Ueda R (2000) The effect of reducing light-harvesting pigment on marine microalgal productivity. J Appl Phycol 12(3–5):285–290
Nakajima Y, Tsuzuki M, Ueda R (2001) Improved productivity by reduction of the content of light-harvesting pigment in Chlamydomonas perigranulata. J Appl Phycol 13(2):95–101
Nath K, Das D (2004) Improvement of fermentative hydrogen production: various approaches. Appl Microbiol Biotechnol 65(5):520–529
Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7(21):3964–3979
Nguyen AV, Thomas-Hall SR, Malnoe A, Timmins M, Mussgnug JH, Rupprecht J, Kruse O, Hankamer B, Schenk PM (2008) Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 7(11):1965–1979
Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Struct Fold Des 7(1):13–23
Nicolet Y, Lemon BJ, Fontecilla-Camps JC, Peters JW (2000) A novel FeS cluster in Fe-only hydrogenases. Trends Biochem Sci 25(3):138–143
Nicolet Y, de Lacey AL, Vernede X, Fernandez VM, Hatchikian EC, Fontecilla-Camps JC (2001) Crystallographic and FTIR spectroscopic evidence of changes in Fe coordination upon reduction of the active site of the Fe-only hydrogenase from Desulfovibrio desulfuricans. J Am Chem Soc 123(8):1596–1601
Nicolet Y, Rubach JK, Posewitz MC, Amara P, Mathevon C, Atta M, Fontecave M, Fontecilla-Camps JC (2008) X-ray structure of the [FeFe]-hydrogenase maturase HydE from Thermotoga maritima. J Biol Chem 283(27):18861–18872
Niu S, Hall MB (2001) Modeling the active sites in metalloenzymes 5. The heterolytic bond cleavage of H2 in the [NiFe] hydrogenase of Desulfovibrio gigas by a nucleophilic addition mechanism. Inorg Chem 40(24):6201–6203
Noike T, Mizuno O (2000) Hydrogen fermentation of organic municipal wastes. Water Sci Technol 42(12):155–162
Ogata H, Mizoguchi Y, Mizuno N, Miki K, Adachi S, Yasuoka N, Yagi T, Yamauchi O, Hirota S, Higuchi Y (2002) Structural studies of the carbon monoxide complex of [NiFe]hydrogenase from Desulfovibrio vulgaris Miyazaki F: suggestion for the initial activation site for dihydrogen. J Am Chem Soc 124(39):11628–11635
Ogata H, Hirota S, Nakahara A, Komori H, Shibata N, Kato T, Kano K, Higuchi Y (2005) Activation process of [NiFe] hydrogenase elucidated by high-resolution X-ray analyses: conversion of the ready to the unready state. Structure 13(11):1635–1642
Ogata H, Lubitz W, Higuchi Y (2009) [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism. Dalton Trans 37:7577–7587
Ohta S, Miyamoto K, Miura Y (1987) Hydrogen evolution as a consumption mode of reducing equivalents in green algal fermentation. Plant Physiol 83:1022–1026
Omoregie E, Crumbliss L, Bebout B, Zehr J (2004) Determination of nitrogen-fixing phylotypes in Lyngbya sp. and Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico. Appl Environ Microbiol 70(4):2119
Pandelia ME, Ogata H, Currell LJ, Flores M, Lubitz W (2009) Inhibition of the [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F by carbon monoxide: an FTIR and EPR spectroscopic study. Biochim Biophys Acta 1797(2):304–313
Pandey AS, Harris TV, Giles LJ, Peters JW, Szilagyi RK (2008) Dithiomethylether as a ligand in the hydrogenase h-cluster. J Am Chem Soc 130(13):4533–4540
Pardo A, De Lacey AL, Fernandez VM, Fan HJ, Fan Y, Hall MB (2006) Density functional study of the catalytic cycle of nickel-iron [NiFe] hydrogenases and the involvement of high-spin nickel(II). J Biol Inorg Chem 11(3):286–306
Paschos A, Glass RS, Bock A (2001) Carbamoylphosphate requirement for synthesis of the active center of [NiFe]-hydrogenases. FEBS Lett 488(1–2):9–12
Paschos A, Bauer A, Zimmermann A, Zehelein E, Bock A (2002) HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturation. J Biol Chem 277(51):49945–49951
Peters JW (1999) Structure and mechanism of iron-only hydrogenases. Curr Opin Struct Biol 9(6):670–676
Peters JW, Szilagyi RK (2006) Exploring new frontiers of nitrogenase structure and mechanism. Curr Opin Chem Biol 10(2):101–108
Peters JW, Stowell MH, Soltis SM, Finnegan MG, Johnson MK, Rees DC (1997) Redox-dependent structural changes in the nitrogenase P-cluster. Biochemistry 36(6):1181–1187
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(5395):1853–1858
Peters JW, Szilagyi RK, Naumov A, Douglas T (2006) A radical solution for the biosynthesis of the H-cluster of hydrogenase. FEBS Lett 580(2):363–367
Pfannschmidt T, Schutze K, Fey V, Sherameti I, Oelmuller R (2003) Chloroplast redox control of nuclear gene expression – a new class of plastid signals in interorganellar communication. Antioxid Redox Signal 5(1):95–101
Pierik AJ, Roseboom W, Happe RP, Bagley KA, Albracht SPJ (1999) Carbon monoxide and cyanide as intrinsic ligands to iron in the active site of [NiFe]-Hydrogenases. NiFe(CN)2CO, biology’s way to activate H2. J Biol Chem 274(6):3331–3337
Pilet E, Nicolet Y, Mathevon C, Douki T, Fontecilla-Camps JC, Fontecave M (2009) The role of the maturase HydG in [FeFe]-hydrogenase active site synthesis and assembly. FEBS Lett 583(3):506–511
Polle JEW, Kanakagiri S, Jin E, Masuda T, Melis A (2002) Truncated chlorophyll antenna size of the photosystems – a practical method to improve microalgal productivity and hydrogen production in mass culture. Int J Hydrogen Energy 27(11–12):1257–1264
Polle JEW, Kanakagiri SD, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217(1):49–59
Posewitz MC, King PW, Smolinski SL, Zhang L, 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(24):25711–25720
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(8):2151–2163
Posewitz MC, King PW, Smolinski SL, Smith RD, Ginley AR, Ghirardi ML, Seibert M (2005) Identification of genes required for hydrogenase activity in Chlamydomonas reinhardtii. Biochem Soc Trans 33(1):102–104
Posewitz MC, Mulder DW, Peters JW (2008) New frontiers in hydrogenase structure and biosynthesis. Curr Chem Biol 2:178–199
Prince RC, Kheshgi HS (2005) The photobiological production of hydrogen: potential efficiency and effectiveness as a renewable fuel. Crit Rev Microbiol 31(1):19–31
Quinn JM, Eriksson M, Moseley JL, Merchant S (2002) Oxygen deficiency responsive gene expression in Chlamydomonas reinhardtii through a copper-sensing signal transduction pathway. Plant Physiol 128(2):463–471
Rangaraj P, Ludden PW (2002) Accumulation of 99Mo-containing iron-molybdenum cofactor precursors of nitrogenase on NifNE, NifH, and NifX of Azotobacter vinelandii. J Biol Chem 277(42):40106–40111
Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21(3):541–554
Redding K, Cournac L, Vassiliev IR, Golbeck JH, Peltier G, Rochaix JD (1999) Photosystem I is indispensable for photoautotrophic growth, CO2 fixation, and H2 photoproduction in Chlamydomonas reinhardtii. J Biol Chem 274(15):10466–10473
Reiher M, Hess BA (2002) A quantum-chemical study of dinitrogen reduction at mononuclear iron-sulfur complexes with hints to the mechanism of nitrogenase. Chemistry 8(23):5332–5339
Reissmann S, Hochleitner E, Wang H, Paschos A, Lottspeich F, Glass RS, Bock A (2003) Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands. Science 299(5609):1067–1070
Reistad R (1970) On the composition and nature of the bulk protein of extremely halophilic bacteria. Arch Mikrobiol 71(4):353–360
Ren NQ, Cao GL, Guo WQ, Wang AJ, Zhu YH, Liu B, Xu JF (2009) Biological hydrogen production from corn stover by moderately thermophile Thermoanaerobacterium thermosaccharolyticum W16. Int J Hydrogen Energy 7:2708–2712
Ribbe M, Gadkari D, Meyer O (1997) N2 fixation by Streptomyces thermoautotrophicus involves a molybdenum-dinitrogenase and a manganese-superoxide oxidoreductase that couple N2 reduction to the oxidation of superoxide produced from O2 by a molybdenum-CO dehydrogenase. J Biol Chem 272(42):26627–26633
Rivera-Ortiz JM, Burris RH (1975) Interactions among substrates and inhibitors of nitrogenase. J Bacteriol 123(2):537–545
Roberts GP, Brill WJ (1980) Gene-product relationships of the nif regulon of Klebsiella pneumoniae. J Bacteriol 144(1):210–216
Rod TH, Norskov JK (2000) Modeling the nitrogenase FeMo cofactor. J Am Chem Soc 122(51):12751–12763
Roessler PG, Lien S (1984) Purification of hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 75(3):705–709
Roll JT, Shah VK, Dean DR, Roberts GP (1995) Characteristics of NIFNE in Azotobacter vinelandii strains. Implications for the synthesis of the iron-molybdenum cofactor of dinitrogenase. J Biol Chem 270(9):4432–4437
Rolland N, Atteia A, Decottignies P, Garin J, Hippler M, Kreimer G, Lemaire SD, Mittag M, Wagner V (2009) Chlamydomonas proteomics. Curr Opin Microbiol 12(3):285–291
Roseboom W, Blokesch M, Bock A, Albracht SP (2005) The biosynthetic routes for carbon monoxide and cyanide in the Ni-Fe active site of hydrogenases are different. FEBS Lett 579(2):469–472
Rossmann R, Sauter M, Lottspeich F, Bock A (1994) Maturation of the large subunit (HYCE) of Escherichia coli hydrogenase 3 requires nickel incorporation followed by C-terminal processing at Arg537. Eur J Biochem 220(2):377–384
Rossmann R, Maier T, Lottspeich F, Bock A (1995) Characterisation of a protease from Escherichia coli involved in hydrogenase maturation. Eur J Biochem 227(1–2):545–550
Rubach JK, Brazzolotto X, Gaillard J, Fontecave M (2005) Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima. FEBS Lett 579(22):5055–5060
Rubio LM, Ludden PW (2002) The gene products of the nif regulon. In: Leigh GJ (ed) Nitrogen fixation at the millennium. Elsevier Science, Amsterdam, pp 101–136
Rubio LM, Ludden PW (2005) Maturation of nitrogenase: a biochemical puzzle. J Bacteriol 187(2):405–414
Rubio LM, Ludden PW (2008) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu Rev Microbiol 62:93–111
Rupprecht J, Hankamer B, Mussgnug JH, Ananyev G, Dismukes C, Kruse O (2006) Perspectives and advances of biological H2 production in microorganisms. Appl Microbiol Biotechnol 72(3):442–449
Russell GK, Gibbs M (1968) Evidence for the participation of the reductive pentose phosphate cycle in photoreduction and the oxyhydrogen reaction. Plant Physiol 43(4):649–652
Rutter J, Reick M, Wu LC, McKnight SL (2001) Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293(5529):510–514
Ryle MJ, Lee H-I, Seefeldt LC, Hoffman BM (2000) Nitrogenase reduction of carbon disulfide: freeze-quench EPR and ENDOR evidence for three sequential intermediates with cluster-bound carbon moieties. Biochemistry 39(5):1114–1119
Saint-Amans S, Girbal L, Andrade J, Ahrens K, Soucaille P (2001) Regulation of carbon and electron flow in Clostridium butyricum VPI 3266 grown on glucose-glycerol mixtures. J Bacteriol 183(5):1748–1754
Sapra R, Bagramyan K, Adams MW (2003) A simple energy-conserving system: proton reduction coupled to proton translocation. Proc Natl Acad Sci USA 100(13):7545–7550
Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J 17(13):3640–3650
Schmitz O, Boison G, Bothe H (2001) Quantitative analysis of expression of two circadian clock-controlled gene clusters coding for the bidirectional hydrogenase in the cyanobacterium Synechococcus sp. PCC7942. Mol Microbiol 41(6):1409–1417
Schmitz O, Boison G, Salzmann H, Bothe H, Schutz K, Wang SH, Happe T (2002) HoxE–a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim Biophys Acta 1554(1–2):66–74
Schonfeld C, Wobbe L, Borgstadt R, Kienast A, Nixon PJ, Kruse O (2004) The nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J Biol Chem 279(48):50366–50374
Schutz K, Happe T, Troshina O, Lindblad P, Leitao E, Oliveira P, Tamagnini P (2004) Cyanobacterial H2 production – a comparative analysis. Planta 218(3):350–359
Seefeldt LC, Dean DR (1997) Role of nucleotides in nitrogenase catalysis. Acc Chem Res 30(6):260–266
Seefeldt L, Dance I, Dean D (2004) Substrate interactions with nitrogenase: Fe versus Mo. Biochemistry 43(6):1401–1409
Seefeldt LC, Hoffman BM, Dean DR (2009) Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem 78:701–722
Semin BK, Davletshina LN, Novakova AA, Kiseleva TY, Lanchinskaya VY, Aleksandrov AY, Seifulina N, Ivanov II, Seibert M, Rubin AB (2003) Accumulation of ferrous iron in Chlamydomonas reinhardtii. Influence of CO2 and anaerobic induction of the reversible hydrogenase. Plant Physiol 131(4):1756–1764
Shah VK, Brill WJ (1977) Isolation of an iron-molybdenum cofactor from nitrogenase. Proc Natl Acad Sci USA 74(8):3249–3253
Shah VK, Allen JR, Spangler NJ, Ludden PW (1994) In vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Purification and characterization of NifB cofactor, the product of NIFB protein. J Biol Chem 269(2):1154–1158
Shepard EM, Mcglynn SE, Bueling A, Grady-Smith C, George S, Winslow MA, Cramer SP, Peters JW, Broderick JB (2010) Synthesis of the 2Fe-subcluster of the [FeFe]-hydrogenase H-cluster on the HydF scaffold. Proc Natl Acad Sci USA 107(23):10448–10453
Siegbahn PEM, Westerberg J, Svensson M, Crabtree RH (1998) Nitrogen fixation by nitrogenases: a quantum chemical study. J Phys Chem B 102(9):1615–1623
Silakov A, Wenk B, Reijerse E, Lubitz W (2009) 14N HYSCORE investigation of the H-cluster of [FeFe] hydrogenase: evidence for a nitrogen in the dithiol bridge. Phys Chem Chem Phys 11(31):6592–6599
Simon DF, Descombes P, Zerges W, Wilkinson KJ (2008) Global expression profiling of Chlamydomonas reinhardtii exposed to trace levels of free cadmium. Environ Toxicol Chem 27(8):1668–1675
Simpson FB, Burris RH (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224(4653):1095–1097
Skjanes K, Knutsen G, Kallqvist T, Lindblad P (2008) H2 production from marine and freshwater species of green algae during sulfur deprivation and considerations for bioreactor design. Int J Hydrogen Energy 33(2):511–521
Soboh B, Linder D, Hedderich R (2004) A multisubunit membrane-bound [NiFe] hydrogenase and an NADH-dependent Fe-only hydrogenase in the fermenting bacterium Thermoanaerobacter tengcongensis. Microbiology 150(7):2451–2463
Soboh B, Igarashi RY, Hernandez JA, Rubio LM (2006) Purification of a NifEN protein complex that contains bound molybdenum and a FeMo-Co precursor from an Azotobacter vinelandii ΔnifHDK strain. J Biol Chem 281(48):36701–36709 Sobah B, Boyd Es, Zhao D, Peters JW, Rubio LM (2010) Substrate specificity and evolutionary implications of a NifDK enzyme carrying NifB-co at its active site. FEBS Lett 584(8):1487–1492 (Epub 2010 Feb 26)
Sorgenfrei O, Klein A, Albracht SP (1993) Influence of illumination on the electronic interaction between 77Se and nickel in active F420-non-reducing hydrogenase from Methanococcus voltae. FEBS Lett 332(3):291–297
Sorlie M, Christiansen J, Dean DR, Hales BJ (1999) Detection of a new radical and FeMo-cofactor EPR signal during acetylene reduction by the α-H195Q mutant of nitrogenase. J Am Chem Soc 121(40):9457–9458
Spencer LP, MacKay BA, Patrick BO, Fryzuk MD (2006) Inner-sphere two-electron reduction leads to cleavage and functionalization of coordinated dinitrogen. Proc Natl Acad Sci USA 103(46):17094–17098
Stauber EJ, Hippler M (2004) Chlamydomonas reinhardtii proteomics. Plant Physiol Biochem 42(12):989–1001
Steppe T, Paerl H (2005) Nitrogenase activity and nifH expression in a marine intertidal microbial mat. Microb Ecol 49(2):315–324
Steunou AS, Bhaya D, Bateson MM, Melendrez MC, Ward DM, Brecht E, Peters JW, Kuhl M, Grossman AR (2006) In situ analysis of nitrogen fixation and metabolic switching in unicellular thermophilic cyanobacteria inhabiting hot spring microbial mats. Proc Natl Acad Sci USA 103(7):2398–2403
Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, Armstrong FA, Happe T (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. Proc Natl Acad Sci USA 106(41):17331–17336
Tamagnini P, Costa JL, Almeida L, Oliveira MJ, Salema R, Lindblad P (2000) Diversity of cyanobacterial hydrogenases, a molecular approach. Curr Microbiol 40(6):356–361
Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wunschiers R, Lindblad P (2002) Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66(1):1–20, table of contents
Tamagnini P, Leitao E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31(6):692–720
Tard C, Pickett CJ (2009) Structural and functional analogues of the active sites of the [Fe]-, [NiFe]-, and [FeFe]-hydrogenases. Chem Rev 109(6):2245–2274
Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, Merchant SS (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284(38):25867–25878
Tetali SD, 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(4):813–829
Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41(1):100–180
Thorneley RN, Lowe DJ (1984) The mechanism of Klebsiella pneumoniae nitrogenase action. Pre-steady-state kinetics of an enzyme-bound intermediate in N2 reduction and of NH3 formation. Biochem J 224(3):887–894
Tolstygina IV, Antal TK, Kosourov SN, Krendeleva TE, Rubin AB, Tsygankov AA (2009) Hydrogen production by photoautotrophic sulfur-deprived Chlamydomonas reinhardtii pre-grown and incubated under high light. Biotechnol Bioeng 102(4):1055–1061
Torzillo G, Scoma A, Faraloni C, Ena A, Johanningmeier U (2009) Increased hydrogen photoproduction by means of a sulfur-deprived Chlamydomonas reinhardtii D1 protein mutant. Int J Hydrogen Energy 34(10):4529–4536
Tosatto S, Toppo S, Carbonera D, Giacometti G, Costantini P (2008) Comparative analysis of [FeFe] hydrogenase from Thermotogales indicates the molecular basis of resistance to oxygen inactivation. Int J Hydrogen Energy 33(2):570–578
Trofanchuk O, Stein M, Gessner C, Lendzian F, Higuchi Y, Lubitz W (2000) Single crystal EPR studies of the oxidized active site of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J Biol Inorg Chem 5(1):36–44
Tsygankov A, Kosourov S, Seibert M, Ghirardi M (2002) Hydrogen photoproduction under continuous illumination by sulfur-deprived, synchronous Chlamydomonas reinhardtii cultures. Int J Hydrogen Energy 27(11–12):1239–1244
van der Zwaan JW, Coremans JM, Bouwens EC, Albracht SP (1990) Effect of 17O2 and 13CO on EPR spectra of nickel in hydrogenase from Chromatium vinosum. Biochim Biophys Acta 1041(2):101–110
van Gastel M, Stein M, Brecht M, Schroder O, Lendzian F, Bittl R, Ogata H, Higuchi Y, Lubitz W (2006) A single-crystal ENDOR and density functional theory study of the oxidized states of the [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J Biol Inorg Chem 11(1):41–51
Van Ooteghem SA, Beer SK, Yue PC (2002) Hydrogen production by the thermophilic bacterium Thermotoga neapolitana. Appl Biochem Biotechnol 98–100:177–189
Van Ooteghem SA, Jones A, Van Der Lelie D, Dong B, Mahajan D (2004) H(2) production and carbon utilization by Thermotoga neapolitana under anaerobic and microaerobic growth conditions. Biotechnol Lett 26(15):1223–1232
Vaupel M, Thauer RK (1998) Two F420-reducing hydrogenases in Methanosarcina barkeri. Arch Microbiol 169(3):201–205
Verhagen MF, O’Rourke T, Adams MW (1999) The hyperthermophilic bacterium, Thermotoga maritima, contains an unusually complex iron-hydrogenase: amino acid sequence analyses versus biochemical characterization. Biochim Biophys Acta 1412(3):212–229
Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107(10):4206–4272
Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6(2):159–188
Vignais PM, Dimon B, Zorin NA, Tomiyama M, Colbeau A (2000) Characterization of the hydrogen-deuterium exchange activities of the energy-transducing HupSL hydrogenase and H-2-signaling HupUV hydrogenase in Rhodobacter capsulatus. J Bacteriol 182(21):5997–6004
Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25(4):455–501
Vincent KA, Cracknell JA, Lenz O, Zebger I, Friedrich B, Armstrong FA (2005a) Electrocatalytic hydrogen oxidation by an enzyme at high carbon monoxide or oxygen levels. Proc Natl Acad Sci USA 102(47):16951–16954
Vincent KA, Parkin A, Lenz O, Albracht SP, Fontecilla-Camps JC, Cammack R, Friedrich B, Armstrong FA (2005b) Electrochemical definitions of O2 sensitivity and oxidative inactivation in hydrogenases. J Am Chem Soc 127(51):18179–18189
Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373(6515):580–587
Volbeda A, Garcin E, Piras C, de Lacey AL, Fernandez VM, Hatchikian EC, Frey M, Fontecilla-Camps JC (1996) Structure of the [NiFe] hydrogenase active site: evidence for biologically uncommon Fe ligands. J Am Chem Soc 118(51):12989–12996
Volbeda A, Montet Y, Vernede X, Hatchikian E, Fontecilla-Camps J (2002) High-resolution crystallographic analysis of Desulfovibrio fructiosovorans [NiFe] hydrogenase. Int J Hydrogen Energy 27(11–12):1449–1461
Volbeda A, Martin L, Cavazza C, Matho M, Faber BW, Roseboom W, Albracht SP, Garcin E, Rousset M, Fontecilla-Camps JC (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10(3):239–249
Voordouw G, Brenner S (1985) Nucleotide sequence of the gene encoding the hydrogenase from Desulfovibrio vulgaris (Hildenborough). Eur J Biochem 148(3):515–520
Wang SC, Frey PA (2007) S-adenosylmethionine as an oxidant: the radical SAM superfamily. Trends Biochem Sci 32(3):101–110
Warnecke F, Luginbuhl P et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450(7169):560–565
Watanabe S, Matsumi R, Arai T, Atomi H, Imanaka T, Miki K (2007) Crystal structures of [NiFe] hydrogenase maturation proteins HypC, HypD, and HypE: insights into cyanation reaction by thiol redox signaling. Mol Cell 27(1):29–40
Watanabe S, Arai T, Matsumi R, Atomi H, Imanaka T, Miki K (2009) Crystal structure of HypA, a nickel-binding metallochaperone for [NiFe] hydrogenase maturation. J Mol Biol 394(3):448–459
Waugh R, Boxer DH (1986) Pleiotropic hydrogenase mutants of Escherichia coli K12: growth in the presence of nickel can restore hydrogenase activity. Biochimie 68(1):157–166
Weaver PF, Lien S, Seibert M (1980) Photobiological production of hydrogen. Solar Energy 24:3–45
White AL, Melis A (2006) Biochemistry of hydrogen metabolism in Chlamydomonas reinhardtii wild type and a Rubisco-less mutant. Int J Hydrogen Energy 31(4):455–464
Winkler M, Heil B, Happe T (2002a) Isolation and molecular characterization of the [Fe]-hydrogenase from the unicellular green alga Chlorella fusca. Biochim Biophys Acta 1576(3):330–334
Winkler M, Hemschemeier A, Gotor C, Melis A, Happe T (2002b) [Fe]-hydrogenases in green algae: photo-fermentation and hydrogen evolution under sulfur deprivation. Int J Hydrogen Energy 27(11–12):1431–1439
Winkler M, Maeurer C, Hemschemeier A, Happe T (2004) The isolation of green algal strains with outstanding H2-productivity. In: Miyake J, Igarashi Y, Rogner M (eds) Biohydrogen III. Elsevier Sci, Oxford, pp 103–115
Winkler M, Kuhlgert S, Hippler M, Happe T (2009) Characterization of the key step for light-driven hydrogen evolution in green algae. J Biol Chem 284(52):36620–36627
Winter HC, Burris RH (1976) Nitrogenase. Annu Rev Biochem 45:409–426
Woodward J, Mattingly SM, Danson M, Hough D, Ward N, Adams M (1996) In vitro hydrogen production by glucose dehydrogenase and hydrogenase. Nat Biotechnol 14(7):872–874
Woodward J, Orr M, Cordray K, Greenbaum E (2000) Enzymatic production of biohydrogen. Nature 405(6790):1014–1015
Wu LF, Mandrand MA (1993) Microbial hydrogenases: primary structure, classification, signatures and phylogeny. FEMS Microbiol Rev 10(3–4):243–269
Wunschiers R, Stangier K, Senger H, Schulz R (2001) Molecular evidence for a Fe-hydrogenase in the green alga Scenedesmus obliquus. Curr Microbiol 42(5):353–360 Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutreient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117(1):129–139
Xia W, Li H, Sze KH, Sun H (2009) Structure of a nickel chaperone, HypA, from Helicobacter pylori reveals two distinct metal binding sites. J Am Chem Soc 131(29):10031–10040
Xing D, Ren N, Rittmann BE (2008) Genetic diversity of hydrogen-producing bacteria in an acidophilic ethanol-H2-coproducing system, analyzed using the [Fe]-hydrogenase gene. Appl Environ Microbiol 74(4):1232–1239
Yandulov DV, Schrock RR (2003) Catalytic reduction of dinitrogen to ammonia at a single molybdenum center. Science 301(5629):76–78
Ye X, Wang Y, Hopkins RC, Adams MW, Evans BR, Mielenz JR, Zhang YH (2009) Spontaneous high-yield production of hydrogen from cellulosic materials and water catalyzed by enzyme cocktails. ChemSusChem 2(2):149–152
Yoon JH, Shin JH, Park TH (2008) Characterization of factors influencing the growth of Anabaena variabilis in a bubble column reactor. Bioresour Technol 99(5):1204–1210
Yoshino F, Ikeda H, Masukawa H, Sakurai H (2007) High photobiological hydrogen production activity of a Nostoc sp. PCC 7422 uptake hydrogenase-deficient mutant with high nitrogenase activity. Mar Biotechnol 9:101–112
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(3):1069–1077
Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214(4):552–561
Zhang JW, Butland G, Greenblatt JF, Emili A, Zamble DB (2005) A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J Biol Chem 280(6):4360–4366
Zhang YH, Evans BR, Mielenz JR, Hopkins RC, Adams MW (2007) High-yield hydrogen production from starch and water by a synthetic enzymatic pathway. PLoS One 2(5):e456
Zhao D, Curatti L, Rubio LM (2007) Evidence for nifU and nifS participation in the biosynthesis of the iron-molybdenum cofactor of nitrogenase. J Biol Chem 282(51):37016–37025
Zinn T, Schnackenberg J, Haak D, Romer S, Schulz R, Senger H (1994) Evidence for nickel in the soluble hydrogenase from the unicellular green alga Scenedesmus obliquus. Z Naturforsch C 49(1–2):33–38
Acknowledgments
The authors would like to thank the U.S. Air Force Office of Scientific Research (MURI award FA9550-05-01-0365); the U.S. Department of Energy’s Office of Science BES and BER programs, the Hydrogen, Fuel Cell and Infrastructure Technologies Program; and the NSF (award 0328187) for support.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Peters, J.W., Boyd, E.S., D’Adamo, S., Mulder, D.W., Therien, J., Posewitz, M.C. (2013). Hydrogenases, Nitrogenases, Anoxia, and H2 Production in Water-Oxidizing Phototrophs. In: Borowitzka, M., Moheimani, N. (eds) Algae for Biofuels and Energy. Developments in Applied Phycology, vol 5. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5479-9_3
Download citation
DOI: https://doi.org/10.1007/978-94-007-5479-9_3
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-5478-2
Online ISBN: 978-94-007-5479-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)