Skip to main content

Advertisement

SpringerLink
Log in

Implementation of photobiological H2 production: the O2 sensitivity of hydrogenases

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The search for the ultimate carbon-free fuel has intensified in recent years, with a major focus on photoproduction of H2. Biological sources of H2 include oxygenic photosynthetic green algae and cyanobacteria, both of which contain hydrogenase enzymes. Although algal and cyanobacterial hydrogenases perform the same enzymatic reaction through metallo-clusters, their hydrogenases have evolved separately, are expressed differently (transcription of algal hydrogenases is anaerobically induced, while bacterial hydrogenases are constitutively expressed), and display different sensitivity to O2 inactivation. Among various physiological factors, the sensitivity of hydrogenases to O2 has been one of the major factors preventing implementation of biological systems for commercial production of renewable H2. This review addresses recent strategies aimed at engineering increased O2 tolerance into hydrogenases (as of now mainly unsuccessful), as well as towards the development of methods to bypass the O2 sensitivity of hydrogenases (successful but still yielding low solar conversion efficiencies). The author concludes with a description of current approaches from various laboratories to incorporate multiple genetic traits into either algae or cyanobacteria to jointly address limiting factors other than the hydrogenase O2 sensitivity and achieve more sustained H2 photoproduction activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abou Hamdan A, Dementin S, Liebgott PP, Gutierrez-Sanz O, Richaud P, De Lacey AL, Rousset M, Bertrand P, Cournac L, Leger C (2012) Understanding and tuning the catalytic bias of hydrogenase (vol 134, p 8368, 2012). J Am Chem Soc 134:9828

    Google Scholar 

  • Adams MW, Mortenson LE (1984) The physical and catalytic properties of hydrogenase II of Clostridium pasteurianum. A comparison with hydrogenase I. J Biol Chem 259:7045–7055

    CAS  PubMed  Google Scholar 

  • Adams MW, Mortenson LE, Chen JS (1980) Hydrogenase. Biochim Biophys Acta 594:105–176

    CAS  PubMed  Google Scholar 

  • 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 1298:141–147

    CAS  PubMed  Google Scholar 

  • Armstrong FA (2004) Hydrogenases: active site puzzles and progress. Curr Opin Chem Biol 8:133–140

    CAS  PubMed  Google Scholar 

  • Armstrong FA, Albracht SP (2005) [NiFe]-hydrogenases: spectroscopic and electrochemical definition of reactions and intermediates. Philos Trans 363:937–954 discussion 1035–1040

    CAS  Google Scholar 

  • Aubert-Jousset E, Cano M, Guedeney G, Richaud P, Cournac L (2011) Role of HoxE subunit in Synechocystis PCC6803 hydrogenase. FEBS J 278:4035–4043

    CAS  PubMed  Google Scholar 

  • 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 64:355–359

    CAS  PubMed  Google Scholar 

  • Bingham AS, Smith PR, Swartz JR (2012a) Evolution of an [FeFe] hydrogenase with decreased oxygen sensitivity. Int J Hydrog Energy 37:2965–2976

    CAS  Google Scholar 

  • Bingham AS, Smith PR, Swartz JR (2012b) Evolution of an [FeFe] hydrogenase with decreased oxygen sensitivity. Int J Hydrog Energy 37:2965–2976

    CAS  Google Scholar 

  • Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, Moser CC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, Sayre RT (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809

    CAS  PubMed  Google Scholar 

  • Boichenko VA, Greenbaum E, Seibert M (2004) Hydrogen production by photosynthetic microorganisms. In: Barber J, Archer MD (eds) Photoconversion of solar energy, molecular to global photosynthesis. Imperial College Press, London, pp 397–452

    Google Scholar 

  • Boison G, Schmitz O, Schmitz B, Bothe H (1998) Unusual gene arrangement of the bidirectional hydrogenase and functional analysis of its diaphorase subunit HoxU in respiration of the unicellular cyanobacterium anacystis nidulans. Curr Microbiol 36:253–258

    CAS  PubMed  Google Scholar 

  • Brand JJ, Wright JN, Lien S (1989) Hydrogen production by eukaryotic algae. Biotechnol Bioeng 33:1482–1488

    CAS  PubMed  Google Scholar 

  • Cano M, Volbeda A, Guedeney G, Aubert-Jousset E, Richaud P, Peltier G, Cournac L (2014) Improved oxygen tolerance of the Synechocystis sp PCC 6803 bidirectional hydrogenase by site-directed mutagenesis of putative residues of the gas diffusion channel. Int J Hydrog Energy 39:16872–16884

    CAS  Google Scholar 

  • 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 84:289–296

    CAS  PubMed  Google Scholar 

  • 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 151:631–640

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 13:1321–1329

    CAS  PubMed  Google Scholar 

  • Cohen J, Kim K, Posewitz M, Ghirardi ML, Schulten K, Seibert M, King P (2005b) Molecular dynamics and experimental investigation of H(2) and O(2) diffusion in [Fe]-hydrogenase. Biochem Soc Trans 33:80–82

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cornish AJ, Gartner K, Yang H, Peters JW, Hegg EL (2011) Mechanism of proton transfer in [FeFe]-hydrogenase from Clostridium pasteurianum. J Biol Chem 286:38341–38347

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 186:1737–1746

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cracknell JA, Vincent KA, Ludwig M, Lenz O, Friedrich B, Armstrong FA (2008) Enzymatic oxidation of H2 in atmospheric O2: the electrochemistry of energy generation from trace H2 by aerobic microorganisms. J Am Chem Soc 130:424–425

    CAS  PubMed  Google Scholar 

  • 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 131:10156–10164

    CAS  PubMed  Google Scholar 

  • Dubini A, Ghirardi ML (2014) Engineering photosynthetic organisms for the production of biohydrogen. PhotosynthRes

  • Ducat DC, Sachdeva G, Silver PA (2011) Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proc Natl Acad Sci USA 108:3941–3946

    PubMed Central  CAS  PubMed  Google Scholar 

  • English CM, Eckert C, Brown K, Seibert M, King PW (2009) Recombinant and in vitro expression systems for hydrogenases: new frontiers in basic and applied studies for biological and synthetic H2 production. Dalton Trans 45:9970–9978

    PubMed  Google Scholar 

  • 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 92:10237–10241

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fargione J, Hill J, Tilman D, Polasky S, Hawthorne P (2008) Land clearing and the biofuel carbon debt. Science 319:1235–1238

    CAS  PubMed  Google Scholar 

  • Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303

    CAS  PubMed  Google Scholar 

  • 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 FEBS 270:2750–2758

    CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gartner K, Lechno-Yossef S, Cornish AJ, Wolk CP, Hegg EL (2012) Expression of Shewanella oneidensis MR-a [FeFe]-hydrogenase genes in Anabaena sp. strain PCC 7120. Appl Environ Microbiol 78:8579–8586

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ghirardi ML, Togasaki RK, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotechnol 63–65:141–151

    PubMed  Google Scholar 

  • Ghirardi ML, Zhang JP, Lee JW, Flynn T, Seibert M, Greenbaum E, Melis A (2000) Microalgae: a green source of renewable H-2. Trends Biotechnol 18:506–511

    CAS  PubMed  Google Scholar 

  • Ghirardi ML, Posewitz MC, Maness P-C, Dubini A, Yu J, Seibert M (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu Rev Plant Biol 58:71–91

    CAS  PubMed  Google Scholar 

  • Ghirardi ML, Dubini A, Yu JP, Maness PC (2009) Photobiological hydrogen-producing systems (vol 38, p. 52, 2009). Chem Soc Rev 38:3505

    CAS  Google Scholar 

  • Ghirardi ML, King PW, Mulder DW, Eckert C, Dubini A, Maness PC, Yu J (2014) Hydrogen production by water biophotolysis. In: Zannoni D, De Philippis R (eds) Microbial bioenergy: hydrogen. Springer, Dordrecht

    Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Goldet G, Brandmayr C, Stripp ST, Happe T, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009) Electrochemical kinetic investigations of the reactions of [FeFe]-hydrogenases with carbon monoxide and oxygen: comparing the importance of gas tunnels and active-site electronic/redox effects. J Am Chem Soc 131:14979–14989

    CAS  PubMed  Google Scholar 

  • Gutekunst K, Chen X, Schreiber K, Kaspar U, Makam S, Appel J (2014) The bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 is reduced by flavodoxin and ferredoxin and is essential under mixotrophic, nitrate-limiting conditions. J Biol Chem 289:1930–1937

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 131:10–21

    CAS  PubMed  Google Scholar 

  • Hanna MC, Nozik AJ (2006) Solar conversion efficiency of photovoltaic and photoelectrolysis cells with carrier multiplication absorbers. J Appl Phys 100:74510(1–8)

    Google Scholar 

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

    CAS  Google Scholar 

  • Healey F (1970) Hydrogen evolution by several algae. Planta 91:220–226

    CAS  PubMed  Google Scholar 

  • Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926

    CAS  PubMed  Google Scholar 

  • 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 227:397–407

    CAS  PubMed  Google Scholar 

  • James BD, Baum GN, Perez J, Baum KN (2009) Technoeconomic boundary analysis of biological pathways to hydrogen production

  • Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuine S, Cournac L, Peltier G, Remacle C, Franck R (2008) A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci USA 105:20546–20551

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jones AK, Sillery E, Albracht SP, Armstrong FA (2002) Direct comparison of the electrocatalytic oxidation of hydrogen by an enzyme and a platinum catalyst. Chem Commun (Camb) 8:866–867

    Google Scholar 

  • Katsuda T, Oshima H, Azuma M, Kato J (2006) New detection method for hydrogen gas for screening hydrogen-producing microorganisms using water-soluble Wilkinson’s catalyst derivative. J Biosci Bioeng 102:220–226

    CAS  PubMed  Google Scholar 

  • Kessler E (1974) Hydrogenase, photoreduction and anaerobic growth. In: Steward WDP (ed) Algal physiology and biochemistry. Blackwell, Oxford, pp 456–473

    Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kosourov S, Seibert M, Ghirardi ML (2003a) Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H-2-producing Chlamydomonas reinhardtii cultures. Plant Cell Physiol 44:146–155

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H2 production in engineered green algal cells. J Biol Chem 280:34170–34177

    CAS  PubMed  Google Scholar 

  • Lambertz C, Leidel N, Havelius KGV, Noth J, Chernev P, Winklers M, Happe T, Haumann M (2011) O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase. J Biol Chem 286:40614–40623

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lamle SE, Albracht SP, Armstrong FA (2005) The mechanism of activation of a [NiFe]-hydrogenase by electrons, hydrogen, and carbon monoxide. J Am Chem Soc 127:6595–6604

    CAS  PubMed  Google Scholar 

  • Laurinavichene T, Tolstygina I, Tsygankov A (2004) The effect of light intensity on hydrogen production by sulfur-deprived Chlamydomonas reinhardtii. J Biotechnol 114:143–151

    CAS  PubMed  Google Scholar 

  • Lee HS, Vermaas WFJ, Rittmann BE (2010) Biological hydrogen production: prospects and challenges. Trends Biotechnol 28:262–271

    CAS  PubMed  Google Scholar 

  • Leger C, Jones AK, Roseboom W, Albracht SP, Armstrong FA (2002) Enzyme electrokinetics: hydrogen evolution and oxidation by Allochromatium vinosum [NiFe]-hydrogenase. Biochemistry 41:15736–15746

    CAS  PubMed  Google Scholar 

  • Leroux F, Dementin S, Burlatt 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 105:11188–11193

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lien S, Pietro AS (1981) Effect of uncouplers on anaerobic adaptation of hydrogenase activity in C. reinhardtii. Biochem Biophys Res Commun 103:139–147

    CAS  PubMed  Google Scholar 

  • Lukey MJ, Roessler MM, Parkin A, Evans RM, Davies RA, Lenz O, Friedrich B, Sargent F, Armstrong FA (2011) Oxygen-tolerant [NiFe]-hydrogenases: the individual and collective importance of supernumerary cysteines at the proximal Fe-S cluster. J Am Chem Soc 133:16881–16892

    CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 94:79–89

    CAS  PubMed  Google Scholar 

  • Maneeruttanarungroj C, Lindblad P, Incharoensakdi A (2010) A newly isolated green alga, Tetraspora sp. CU2551, from Thailand with efficient hydrogen production. Int J Hydrog Energy 35:13193–13199

    CAS  Google Scholar 

  • 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 68:2633–2636

    PubMed Central  CAS  PubMed  Google Scholar 

  • Markov SA, Eivazova ER, Greenwood J (2006) Photostimulation of H-2 production in the green alga Chlamydomonas reinhardtii upon photoinhibition of its O-2-evolving system. Int J Hydrog Energy 31:1314–1317

    CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Meuser JE, D’Adamo S, Jinkerson RE, Mus F, Yang W, Ghirardi ML, Seibert M, Grossman AR, Posewitz MC (2012a) Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: insight into the role of HYDA2 in H(2) production. Biochem Biophys Res Commun 417:704–709

    CAS  PubMed  Google Scholar 

  • Meuser JE, D’Adamo S, Jinkerson RE, Mus F, Yang WQ, Ghirardi ML, Seibert M, Grossman AR, Posewitz MC (2012b) Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: insight into the role of HYDA2 in H-2 production. Biochem Biophys Res Commun 417:704–709

    CAS  PubMed  Google Scholar 

  • 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 4:523–526

    CAS  PubMed  Google Scholar 

  • Mulder DW, Boyd ES, Sarma R, Lange RK, Endrizzi JA, Broderick JB, Peters JW (2010) Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydA(Delta EFG). Nature 465:248-U143

  • Mulder DW, Ratzloff MW, Shepard EM, Byer AS, Noone SM, Peters JW, Broderick JB, King PW (2013) EPR and FTIR analysis of the mechanism of H2 activation by [FeFe]-hydrogenase HydA1 from Chlamydomonas reinhardtii. J Am Chem Soc 135:6921–6929

    CAS  PubMed  Google Scholar 

  • 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. Structure 7:13–23

    CAS  PubMed  Google Scholar 

  • Oey M, Ross I, Stephens E, Steinbeck J, Wolf J, Radzun K, Kugler J, Ringsmuth A, Kruse O, Hankamer B (2013) RNAi knock-down of LHCBM1, 2 and 3 increases photosynthetic H2 production efficiency of the green alga Chlamydomonas reinhardtii. PLoS ONE 8:e61375

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pandelia ME, Nitschke W, Infossi P, Giudici-Orticoni MT, Bill E, Lubitz W (2011) Characterization of a unique [FeS] cluster in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus. Proc Natl Acad Sci USA 108:6097–6102

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Philipps G, Happe T, Hemschemeier A (2012) Nitron deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235:729–745

    CAS  PubMed  Google Scholar 

  • 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 279:25711–25720

    CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Posewitz M, Dubini A, Meuser JE, Seibert M, Ghirardi ML (2008) Hydrogenases, hydrogen production, and anoxia. Chlamydomonas Sourceb 2:215–255

    Google Scholar 

  • Reifschneider-Wegner K, Kanygin A, Redding KE (2014) Expression of the [FeFe hydrogenase in the chloroplast of Chlamydomonas reinhardtii. Int J Hydrog Energy 39:3657–3665

    CAS  Google Scholar 

  • Roessler P, Lien S (1984) Purification of hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 75:705–709

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ruhle T, Hemschemeier A, Melis A, Happe T (2008) A novel screening protocol for the isolation of hydrogen producing Chlamydomonas reinhardtii strains. BMC Plant Biol 8:107

    PubMed Central  PubMed  Google Scholar 

  • Rupprecht J (2009) From systems biology to fuel–Chlamydomonas reinhardtii as a model for a systems biology approach to improve biohydrogen production. J Biotechnol 142:10–20

    CAS  PubMed  Google Scholar 

  • Schmitz O, Bothe H (1996) The diaphorase subunit HoxU of the bidirectional hydrogenase as electron transferring protein in cyanobacterial respiration? Die Naturwissenschaften 83:525–527

    CAS  PubMed  Google Scholar 

  • Schrader PS, Burrows EH, Ely RL (2008) High-throughput screening assay for biological hydrogen production. Anal Chem 80:4014–4019

    CAS  PubMed  Google Scholar 

  • Scoma A, Krawietz D, Faraloni C, Giannelli L, Happe T, Torzillo G (2012) Sustained H2 production in Chlamydomonas reinhardtii D1 protein mutant. J Biotechnol 157:613–619

    CAS  PubMed  Google Scholar 

  • Searchinger T, Heimlich R, Houghton RA, Dong F, Elobeid A, Fabiosa J, Tokgoz S, Hayes D, Yu TH (2008) Use of US croplands for biofuels increases greenhouse gases through emissions from land-use change. Science 319:1238–1240

    CAS  PubMed  Google Scholar 

  • Seibert M, Flynn T, Benson D, Tracy E, Ghirardi ML (1998) Development of selection/screening procedures for rapid identification of H2-producing algal mutants with increased O2-tolerance. In: Zaborsky OR (ed) Biohydrogen. Plenum Publishing Corporation, New York, pp 227–234

    Google Scholar 

  • Seibert M, Flynn T, Ghirardi ML (2001a) Strategies for improving oxygen tolerance of algal hydrogen production. In: Miyake J, Matsunaga T, Pietro AS (eds) BioHydrogen II. Pergamon Press, Amsterdam, pp 65–76

    Google Scholar 

  • Seibert M, Benson DK, Flynn TM (2001) Method and apparatus for rapid biohydrogen phenotypic screening of microorganisms using a chemochromic sensor. US Patent

  • Shestakov SV, Mikheeva LE (2006) Genetic control of hydrogen metabolism in cyanobacteria. Russ J Genet 42:1272–1284

    CAS  Google Scholar 

  • Skjanes K, Knutsen G, Kallqvist T, Lindblad P (2008) H-2 production from marine and freshwater species of green algae during sulfur deprivation and considerations for bioreactor design. Int J Hydrog Energy 33:511–521

    CAS  Google Scholar 

  • Stapleton JA, Swartz JR (2010a) Development of an in vitro compartmentalization screen for high-throughput directed evolution of [FeFe] hydrogenases. PLoS ONE 5:e15275

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stapleton JA, Swartz JR (2010b) A cell-free microtiter plate screen for improved [FeFe] hydrogenases. PLoS ONE 5:e10554

    PubMed Central  PubMed  Google Scholar 

  • Stripp ST, Happe T (2009) How algae produce hydrogen—news from the photosynthetic hydrogenase. Dalton Trans 45:9960–9969

    PubMed  Google Scholar 

  • 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 106:17331–17336

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sumner I, Both GA (2012) Proton transport pathways in [NiFe]-hydrogenase. J Phys Chem B 116:2917–2926

    CAS  PubMed  Google Scholar 

  • Surzycki R, Cournac L, Peltier G, Rochaix JD (2007) Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas. Proc Natl Acad Sci USA 104:17548–17553

    PubMed Central  CAS  PubMed  Google Scholar 

  • Timmins M, Thomas-Hall SR, Darling A, Zhang E, Hankamer B, Marx UC, Schenk PM (2009) Phylogenetic and molecular analysis of hydrogen-producing green algae. J Exp Bot 60:1691–1702

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I, Krawietz D, Happe T, Auroy P, Adriano JM, Beyly A, Cuine S, Plet J, Reiter IM, Genty B, Cournac L, Hippler M, Peltier G (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–2630

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 102:1055–1061

    CAS  PubMed  Google Scholar 

  • Torzillo G, Scoma A, Faraloni C, Ena E, Johanningmeier U (2009) Increased hydrogen photoproduction by means of a sulfur-deprived Chlamydomonas reinhardtii D1 protein mutant. Int J Hydrog Energy 34:4529–4536

    CAS  Google Scholar 

  • Vignais PM, Colbeau A, Willison JC, Jouanneau Y (1985) Hydrogenase, nitrogenase, and hydrogen metabolism in the photosynthetic bacteria. Adv Microb Physiol 26:155–234

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Vincent KA, Armstrong FA (2005) Investigating metalloenzyme reactions using electrochemical sweeps and steps: fine control and measurements with reactants ranging from ions to gases. Inorg Chem 44:798–809

    CAS  PubMed  Google Scholar 

  • Vincent KA, Cracknell JA, Parkin A, Armstrong FA (2005a) Hydrogen cycling by enzymes: electrocatalysis and implications for future energy technology. Dalton Trans 21:3397–3403

    PubMed  Google Scholar 

  • 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 127:18179–18189

    CAS  PubMed  Google Scholar 

  • Vincent KA, Parkin A, Armstrong FA (2007) Investigating and exploiting the electrocatalytic properties of hydrogenases. Chem Rev 107:4366–4413

    CAS  PubMed  Google Scholar 

  • von Abendroth G, Stripp ST, Silakov A, Croux C, Soucaille P, Girbal L, Happe T (2008) Optimized over-expression of [FeFe] hydrogenases with high specific activity in Clostridium acetobutylicum. Int J Hydrog Energy 33:6076–6081

    Google Scholar 

  • Walker DA (2009) Biofuels, facts, fantasy and feasibility. J Appl Phycol 21:509–517

    Google Scholar 

  • Wang H, Fan X, Zhang Y, Yang D, Guo R (2011) Sustained photo-hydrogen production by Chlorella pyrenoidosa without sulfur depletion. Biotechnol Lett 33:1345–1350

    CAS  PubMed  Google Scholar 

  • Weaver PF, Lien S, Seibert M (1980) Photobiological production of hydrogen. Sol Energy 24:3–45

    CAS  Google Scholar 

  • Wecker MS, Ghirardi ML (2014) High-throughput biosensor discriminates between different algal H2-photoproducing strains. Biotechnol Bioeng 111:1332–1340

    CAS  PubMed  Google Scholar 

  • Wecker MSA, Meuser JE, Posewitz MC, Ghirardi ML (2011) Design of a new biosensor for algal H2 production based on the H2-sensing system of Rhodobacter capsulatus. Int J Hydrog Energy 36:11229–11237

    CAS  Google Scholar 

  • Weyman PD, Vargas WA, Tong Y, Yu J, Maness PC, Smith HO, Xu Q (2011) Heterologous expression of Alteromonas macleodii and Thiocapsa roseopersicina [NiFe] hydrogenases in Synechococcus elongatus. PLoS ONE 6:e20126

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • 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 284:36620–36627

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wu S, Xu L, Huang R, Xang Q (2011) Improved biohydrogen production with an expression of codon-optrimized hemH and lba genes in the chloroplast of Chlamydomonas reinhardtii. Bioresour Technol 102:2610–2616

    CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The author would like to acknowledge support from the U.S. DOE’s Office of Science BER and BES, and from the EERE’s Fuel Cell Technologies Office. The U.S. Government retains and the publisher, by accepting the article for publication, acknowledges that the U.S. Government retains a nonexclusive, paid up, irrevocable, worldwide license to publish or reproduce the published form of this work, or allow others to do so, for U.S. Government purposes.

Conflict of interest

The author declares that she has no conflict of interest.

Author information

Authors and Affiliations

  1. National Renewable Energy Laboratory, 15013 Denver West Pkway, Golden, CO, 80401, USA

    Maria L. Ghirardi

Authors
  1. Maria L. Ghirardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria L. Ghirardi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghirardi, M.L. Implementation of photobiological H2 production: the O2 sensitivity of hydrogenases. Photosynth Res 125, 383–393 (2015). https://doi.org/10.1007/s11120-015-0158-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0158-1

Keywords

Search

Navigation