Hydrogenases and Hydrogen Metabolism of Cyanobacteria

SUMMARY Cyanobacteria may possess several enzymes that are directly involved in dihydrogen metabolism: nitrogenase(s) catalyzing the production of hydrogen concomitantly with the reduction of dinitrogen to ammonia, an uptake hydrogenase (encoded by hupSL) catalyzing the consumption of hydrogen produced by the nitrogenase, and a bidirectional hydrogenase (encoded by hoxFUYH) which has the capacity to both take up and produce hydrogen. This review summarizes our knowledge about cyanobacterial hydrogenases, focusing on recent progress since the first molecular information was published in 1995. It presents the molecular knowledge about cyanobacterial hupSL and hoxFUYH, their corresponding gene products, and their accessory genes before finishing with an applied aspect—the use of cyanobacteria in a biological, renewable production of the future energy carrier molecular hydrogen. In addition to scientific publications, information from three cyanobacterial genomes, the unicellular Synechocystis strain PCC 6803 and the filamentous heterocystous Anabaena strain PCC 7120 and Nostoc punctiforme (PCC 73102/ATCC 29133) is included.

[1]  D. Bryant,et al.  Growth on Urea Can Trigger Death and Peroxidation of the Cyanobacterium Synechococcus sp. Strain PCC 7002 , 1998, Applied and Environmental Microbiology.

[2]  M. Houghton,et al.  Heterocyst Pattern Formation Controlled by a Diffusible Peptide , 1998 .

[3]  J. Dernedde,et al.  Carboxyl-terminal processing of the cytoplasmic NAD-reducing hydrogenase of Alcaligenes eutrophus requires the hoxW gene product , 1996, Journal of bacteriology.

[4]  J. Hackstein,et al.  A hydrogenosome with a genome , 1998, Nature.

[5]  D. Borthakur,et al.  The use of a PCR cloning and screening strategy to identify lambda clones containing the hupB gene of Anabaena sp. strain PCC7120 , 1996 .

[6]  R. Schulz,et al.  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). , 1996, Biochimica et biophysica acta.

[7]  R. Haselkorn,et al.  Deletion of a 55-kilobase-pair DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120 , 1988, Journal of bacteriology.

[8]  B. Masepohl,et al.  The heterocyst-specific fdxH gene product of the cyanobacterium Anabaena sp. PCC 7120 is important but not essential for nitrogen fixation , 1997, Molecular and General Genetics MGG.

[9]  J. Meyer,et al.  Classification and phylogeny of hydrogenases. , 2001, FEMS microbiology reviews.

[10]  J. W. Golden,et al.  Two heterocyst-specific DNA rearrangements of nif operons in Anabaena cylindrica and Nostoc sp. strain Mac. , 1995, Microbiology.

[11]  Takakazu Kaneko,et al.  CyanoBase, a www database containing the complete nucleotide sequence of the genome of Synechocystis sp. strain PCC6803 , 1998, Nucleic Acids Res..

[12]  A. Kumar,et al.  CARBON NUTRITION AND THE REGULATION OF UPTAKE HYDROGENASE ACTIVITY IN FREE-LIVING AND SYMBIOTIC ANABAENA CYCADEAE. , 1986, The New phytologist.

[13]  Cyanobacteria and their symbionts. , 1991 .

[14]  T. Friedrich,et al.  Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. , 1997, Journal of theoretical biology.

[15]  W. Orme-Johnson,et al.  Nitrogenase structure: where to now? , 1992, Science.

[16]  A. Muro-Pastor,et al.  Nitrogen Control in Cyanobacteria , 2001, Journal of bacteriology.

[17]  J. Komárek,et al.  Modern approach to the classification system of cyanophytes 5. stigonematales , 1990 .

[18]  D. Hall,et al.  Hydrogen photoproduction by three different nitrogenases in whole cells of Anabaena variabilis and the dependence on pH , 1997 .

[19]  A. Böck,et al.  Carbamoylphosphate requirement for synthesis of the active center of [NiFe]‐hydrogenases , 2001, FEBS letters.

[20]  Geoffrey D. Smith,et al.  THE HYDROGEN METABOLISM OF CYANOBACTERIA (BLUE‐GREEN ALGAE) , 1981 .

[21]  D. Capone,et al.  The nitrogen physiology of the marine N2-fixing cyanobacteria Trichodesmium spp. , 2000, Trends in plant science.

[22]  T. Friedrich,et al.  The proton‐pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts , 1995, FEBS letters.

[23]  W. Vermaas,et al.  Subunits of the NAD(P)-Reducing Nickel-Containing Hydrogenase Do Not Act as Part of theType-1 NAD(P)H-Dehydrogenase in the Cyanobacterium Synechocystis sp. PCC 6803 , 1999 .

[24]  K. Shanmugam,et al.  Regulation of hydrogenase activity in vegetative cells of Anabaena variabilis , 1983, Journal of bacteriology.

[25]  F. Stejskal,et al.  The Azotobacter chroococcum hydrogenase gene cluster: sequences and genetic analysis of four accessory genes, hupA, hupB, hupY and hupC. , 1993, Gene.

[26]  F. Mayer,et al.  Localization of the Reversible Hydrogenase in Cyanobacteria , 1989 .

[27]  L. Sayavedra-Soto,et al.  Substitution of Azotobacter vinelandii hydrogenase small-subunit cysteines by serines can create insensitivity to inhibition by O2 and preferentially damages H2 oxidation over H2 evolution , 1995, Journal of Bacteriology.

[28]  H. Bothe,et al.  Unusual Gene Arrangement of the Bidirectional Hydrogenase and Functional Analysis of Its Diaphorase Subunit HoxU in Respiration of the Unicellular Cyanobacterium Anacystis nidulans , 1998, Current Microbiology.

[29]  R. Schulz,et al.  Hydrogenases and hydrogen production in eukaryotic organisms and cyanobacteria , 1996 .

[30]  J. Gallon,et al.  Effects of inorganic nitrogen compounds on the activity and synthesis of nitrogenase in Gloeothece (Nägeli) sp. ATCC 27152 , 1999 .

[31]  P. Lindblad,et al.  Immunological characterization of hydrogenases in the nitrogen-fixing cyanobacterium Nostoc sp. strain PCC 73102 , 1995, Current Microbiology.

[32]  P. Böger,et al.  [47] Nitrogen and hydrogen metabolism: Induction and measurement , 1988 .

[33]  F. Lottspeich,et al.  Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria. , 1995, European journal of biochemistry.

[34]  R. Burris,et al.  Occurrence and localization of two distinct hydrogenases in the heterocystous cyanobacterium Anabaena sp. strain 7120 , 1981, Journal of bacteriology.

[35]  D. Hall,et al.  H(2) photoproduction by batch culture of Anabaena variabilis ATCC 29413 and its mutant PK84 in a photobioreactor. , 1999, Biotechnology and bioengineering.

[36]  Y. Asada,et al.  Heterologous expression of clostridial hydrogenase in the Cyanobacterium synechococcus PCC7942. , 2000, Biochimica et biophysica acta.

[37]  H. Bothe,et al.  The utilization of molecular hydrogen by the blue-green alga Anabaena cylindrica , 1977, Archives of Microbiology.

[38]  H. D. Kumar,et al.  Nitrogen fixation and hydrogen uptake in four cyanobacteria , 1995 .

[39]  P. Lindblad,et al.  Towards optimization of cyanobacteria as biotechnologically relevant producers of molecular hydrogen, a clean and renewable energy source , 1998, Applied Microbiology and Biotechnology.

[40]  T. Wei,et al.  Anabaena sp. strain PCC 7120 ntcA gene required for growth on nitrate and heterocyst development , 1994, Journal of bacteriology.

[41]  D. Mazel,et al.  Highly repetitive DNA sequences in cyanobacterial genomes , 1990, Journal of bacteriology.

[42]  D. Bhattacharya Origins of Algae and their Plastids , 1997, Plant Systematics and Evolution.

[43]  G. Smith,et al.  Soluble hydrogenase of Anabaena cylindrica. Cloning and sequencing of a potential gene encoding the tritium exchange subunit. , 1990, European journal of biochemistry.

[44]  L. Stal Physiological ecology of cyanobacteria in microbial mats and other communities. , 1995, The New phytologist.

[45]  T. Happe,et al.  A Novel Type of Iron Hydrogenase in the Green AlgaScenedesmus obliquus Is Linked to the Photosynthetic Electron Transport Chain* , 2001, The Journal of Biological Chemistry.

[46]  J. Meeks,et al.  Elements interrupting nitrogen fixation genes in cyanobacteria: presence and absence of a nifD element in clones of Nostoc sp. strain Mac , 1994 .

[47]  S. Albracht Nickel hydrogenases: in search of the active site. , 1994, Biochimica et biophysica acta.

[48]  P. Lindblad,et al.  Evidence against a common use of the diaphorase subunits by the bidirectional hydrogenase and by the respiratory complex I in cyanobacteria , 1999 .

[49]  H. D. Peck,et al.  Structure-function relationships among the nickel-containing hydrogenases. , 1992, FEMS microbiology reviews.

[50]  Y. Asada,et al.  Hydrogen Evolution by Microcystis aeruginosa in Darkness , 1984 .

[51]  D. Hall,et al.  The potential of using cyanobacteria in photobioreactors for hydrogen production , 1995 .

[52]  G. Peschek,et al.  The Phototrophic Prokaryotes , 1999, Springer US.

[53]  James W. Golden,et al.  PatS and Products of Nitrogen Fixation Control Heterocyst Pattern , 2001, Journal of bacteriology.

[54]  H. Bothe,et al.  The Number of Hydrogenases in Cyanobacteria , 1981 .

[55]  J. W. Golden,et al.  Programmed DNA rearrangement of a cyanobacterial hupL gene in heterocysts. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[56]  L. Casalot,et al.  Maturation of the [NiFe] hydrogenases. , 2001, Trends in microbiology.

[57]  Y. Asada,et al.  Hydrogenase from the unicellular cyanobacterium, Microcystis aeruginosa , 1987 .

[58]  H. Bothe,et al.  Evidence for the occurrence of the alternative, vanadium-containing nitrogenase in the cyanobacterium Anabaena variabilis , 1988 .

[59]  A. Böck,et al.  Dissection of the maturation reactions of the [NiFe] hydrogenase 3 from Escherichia coli taking place after nickel incorporation , 2000, FEBS letters.

[60]  J. Palacios,et al.  Nucleotide sequence and characterization of four additional genes of the hydrogenase structural operon from Rhizobium leguminosarum bv. viciae , 1992, Journal of bacteriology.

[61]  S. Turner Molecular systematics of oxygenic photosynthetic bacteria , 1997 .

[62]  E. Flores,et al.  Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC7120 , 1994, Molecular microbiology.

[63]  Robert Haselkorn,et al.  Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena , 1985, Nature.

[64]  P. Lindblad,et al.  Transcriptional regulation of Nostoc uptake hydrogenase. , 1999, FEMS microbiology letters.

[65]  A. Pierik,et al.  Biological activation of hydrogen. , 1997, Nature.

[66]  A. Daday,et al.  The effect of nickel on hydrogen metabolism and nitrogen fixation in the cyanobacterium Anabaena cylindrica , 1985 .

[67]  K. Shanmugam,et al.  Photodissimilation of Fructose to H(inf2) and CO(inf2) by a Dinitrogen-Fixing Cyanobacterium, Anabaena variabilis , 1996, Applied and environmental microbiology.

[68]  B. Whitton,et al.  Proposal to Place the Nomenclature of the Cyanobacteria (Blue-Green Algae) Under the Rules of the International Code of Nomenclature of Bacteria , 1978 .

[69]  R. Cammack Splitting molecular hydrogen , 1995, Nature.

[70]  D. Bryant The Molecular Biology of Cyanobacteria , 1994, Advances in Photosynthesis.

[71]  J. W. Golden,et al.  Anabaena xisF gene encodes a developmentally regulated site-specific recombinase. , 1994, Genes & development.

[72]  R. Maier,et al.  Requirement of nickel metabolism proteins HypA and HypB for full activity of both hydrogenase and urease in Helicobacter pylori , 2001, Molecular microbiology.

[73]  M. Chu,et al.  Organization and expression of nitrogen-fixation genes in the aerobic nitrogen-fixing unicellular cyanobacterium Synechococcus sp. strain RF-1. , 1999, Microbiology.

[74]  A. Wilmotte Molecular Evolution and Taxonomy of the Cyanobacteria , 1994 .

[75]  Datta Madamwar,et al.  Cyanobacterial hydrogen production , 2000 .

[76]  P. Lindblad,et al.  Induction of H2-Uptake and Nitrogenase Activities in the Cyanobacterium Anabaena variabilis ATCC 29413: Effects of Hydrogen and Organic Substrate , 1996, Current Microbiology.

[77]  K. Anagnostidis Modern approach to the classification system of cyanophytes 1-Introduction. , 1985 .

[78]  G. Codd,et al.  The Uptake and Production of Molecular Hydrogen by Unicellular Cyanobacteria , 1985 .

[79]  D. Hall,et al.  The potential applications of cyanobacterial photosynthesis for clean technologies , 1995, Photosynthesis Research.

[80]  B. Bergman,et al.  Chemical signalling in cyanobacterial-plant symbioses , 1996 .

[81]  P. Vignais,et al.  Molecular biology of membrane bound H2 uptake hydrogenases , 2004, Archives of Microbiology.

[82]  R. Tuli,et al.  Differential expression of photosynthesis and nitrogen fixation genes in the cyanobacterium Plectonema boryanum. , 2000, Plant physiology.

[83]  R. Garg,et al.  The hypE gene completes the gene cluster for H2-oxidation in Azotobacter vinelandii. , 1994, Journal of molecular biology.

[84]  R. Hausinger Metallocenter assembly in nickel-containing enzymes , 1997, JBIC Journal of Biological Inorganic Chemistry.

[85]  I. Bancroft,et al.  Oriented degradation of the genome of cyanophage AN‐23 after exposure to NaCl , 1992 .

[86]  D. Borthakur,et al.  Organization of the hupDEAB genes within the hydrogenase gene cluster of Anabaena sp. strain PCC7120 , 1998, Journal of Applied Phycology.

[87]  P. Vignais,et al.  HupUV proteins of Rhodobacter capsulatus can bind H2: evidence from the H-D exchange reaction , 1997, Journal of bacteriology.

[88]  J. Komárek,et al.  Modern approach to the classification system of Cyanophytes 4 - Nostocales , 1989 .

[89]  C. Nakamura,et al.  Molecular handling of hydrogenase , 2001 .

[90]  P. Lindblad,et al.  Reversible hydrogenase in Anabaena variabilis ATCC 29413 , 1994, Archives of Microbiology.

[91]  J. Benemann,et al.  Hydrogen biotechnology: Progress and prospects , 1996, Nature Biotechnology.

[92]  Michel Frey,et al.  Crystal structure of the nickel–iron hydrogenase from Desulfovibrio gigas , 1995, Nature.

[93]  P. Lindblad,et al.  Hydrogenases in Nostoc sp. Strain PCC 73102, a Strain Lacking a Bidirectional Enzyme , 1997, Applied and environmental microbiology.

[94]  J. Guest,et al.  FNR and its role in oxygen-regulated gene expression in Escherichia coli. , 1990, FEMS microbiology reviews.

[95]  P. Vignais,et al.  The hupTUV operon is involved in negative control of hydrogenase synthesis in Rhodobacter capsulatus , 1996, Journal of bacteriology.

[96]  G. Peschek,et al.  Anaerobic hydrogenase activity in Anacystis nidulans. H2-dependent photoreduction and related reactions. , 1979, Biochimica et biophysica acta.

[97]  H. Bothe,et al.  The Expression of a Third Nitrogenase in the Cyanobacterium Anabaena variabilis , 1991 .

[98]  P. Fay Oxygen relations of nitrogen fixation in cyanobacteria. , 1992, Microbiological reviews.

[99]  J. P. Houchins The physiology and biochemistry of hydrogen metabolism in cyanobacteria , 1984 .

[100]  W. Brill Symbiotic Associations , 1976, Science.

[101]  M. Dilworth,et al.  Biology and biochemistry of nitrogen fixation , 1991 .

[102]  R. Schulz,et al.  HYDROGEN METABOLISM IN ORGANISMS WITH OXYGENIC PHOTOSYNTHESIS : HYDROGENASES AS IMPORTANT REGULATORY DEVICES FOR A PROPER REDOX POISING? , 1998 .

[103]  H. D. Peck,et al.  Cloning, characterization, and sequencing of the genes encoding the large and small subunits of the periplasmic [NiFe]hydrogenase of Desulfovibrio gigas. , 1987, DNA.

[104]  Brenda S. Pratte,et al.  Effect on Heterocyst Differentiation of Nitrogen Fixation in Vegetative Cells of the Cyanobacterium Anabaena variabilisATCC 29413 , 2001, Journal of bacteriology.

[105]  B. Bergman,et al.  Tansley Review No. 116: Cyanobacterium-plant symbioses. , 2000, The New phytologist.

[106]  R. Maier,et al.  Dual Roles of Bradyrhizobium japonicumNickelin Protein in Nickel Storage and GTP-Dependent Ni Mobilization , 2000, Journal of bacteriology.

[107]  G. Peschek,et al.  Aerobic hydrogenase activity in Anacystis nidulans. The oxyhydrogen reaction. , 1979, Biochimica et biophysica acta.

[108]  T. Schmülling,et al.  Hydrogenase activities in cyanobacteria. , 1986, Biochimie.

[109]  Paula Tamagnini,et al.  Diversity of Cyanobacterial Hydrogenases, a Molecular Approach , 2000, Current Microbiology.

[110]  A. Ernst,et al.  Heterocyst Metabolism and Development , 1994 .

[111]  T. Thiel Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis , 1993, Journal of bacteriology.

[112]  J. Meeks [8] Symbiotic associations , 1988 .

[113]  D. Hall,et al.  [53] Hydrogenases: Isolation and assay , 1988 .

[114]  Frank McCormick,et al.  The GTPase superfamily: conserved structure and molecular mechanism , 1991, Nature.

[115]  Geoffrey D. Smith,et al.  Immunochemical analysis of the soluble hydrogenase from the cyanobacterium Anabaena cylindrica , 1989 .

[116]  A. Böck,et al.  Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli , 1991, Molecular microbiology.

[117]  Lucas J. Stal,et al.  Fermentation in cyanobacteria , 1997 .

[118]  M. Tredici,et al.  Heterotrophic metabolism and regulation of uptake hydrogenase activity in symbiotic cyanobacteria , 1991, Plant and Soil.

[119]  Y. Nakamura,et al.  Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement). , 1996, DNA research : an international journal for rapid publication of reports on genes and genomes.

[120]  J. Gallon,et al.  Synthesis and proteolytic degradation of nitrogenase in cultures of the unicellular cyanobacterium Gloeothece strain ATCC 27152. , 1999, Microbiology.

[121]  F. Tabita,et al.  Nickel Control of Hydrogen Production and Uptake in Anabaena spp. Strains CA and 1F , 1984 .

[122]  A. Pierik,et al.  Biological activition of hydrogen , 1997, Nature.

[123]  D. Hall,et al.  Isolation and characterization of the hydrogenase activity from the non‐heterocystous cyanobacterium Spirulina maxima , 1979, FEBS letters.

[124]  A. Ernst,et al.  A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[125]  D. Hall,et al.  The biotechnology of hydrogen production by Nostoc flagelliforme grown under chemostat conditions , 1997, Applied Microbiology and Biotechnology.

[126]  E. Munn,et al.  Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. , 1986, The Biochemical journal.

[127]  Molecular Evidence for a Fe-Hydrogenase in the Green Alga Scenedesmus obliquus , 2001, Current Microbiology.

[128]  R. Haselkorn,et al.  Different recombination site specificity of two developmentally regulated genome rearrangements , 1987, Nature.

[129]  R. Haselkorn,et al.  Bacterial-type ferredoxin genes in the nitrogen fixation regions of the cyanobacterium Anabaena sp. strain PCC 7120 and Rhizobium meliloti , 1988, Journal of bacteriology.

[130]  W. Silvester,et al.  Interactions of H2 and carbon metabolism in moderating nitrogenase activity of the Gunnera/Nostoc symbiosis , 1994, Archives of Microbiology.

[131]  G. Voordouw Evolution of Hydrogenase Genes , 1992 .

[132]  R. Burris,et al.  Comparative characterization of two distinct hydrogenases from Anabaena sp. strain 7120 , 1981, Journal of bacteriology.

[133]  P. Lindblad,et al.  Construction of Transconjugable Plasmids for Use in the Insertion Mutagenesis of Nostoc PCC 73102 Uptake Hydrogenase , 1998 .

[134]  L. E. Mikheeva,et al.  Mutants of the Cyanobacterium Anabaena variabilis Altered in Hydrogenase Activities , 1995 .

[135]  J. Naber,et al.  Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. , 1994, European journal of biochemistry.

[136]  M. Field,et al.  Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics , 1997, Nature Structural Biology.

[137]  P. Luisi,et al.  Surfactant-Induced hydrogen production in cyanobacteria. , 1993, Biotechnology and bioengineering.

[138]  M. E. Mulligan,et al.  Characterization of a nitrogen-fixation (nif) gene cluster from Anabaena azollae 1a shows that closely related cyanobacteria have highly variable but structured intergenic regions. , 1995, Microbiology.

[139]  P. Böger,et al.  Pathways of hydrogen uptake in the cyanobacterium Nostoc muscorum , 1985, Archives of Microbiology.

[140]  P. Lindblad,et al.  Nostoc PCC 73102 and H2 , 1998 .

[141]  D. Hall,et al.  Acetylene reduction and hydrogen photoproduction by wild-type and mutant strains of Anabaena at different CO2 and O2 concentrations , 1998 .

[142]  G. Smith,et al.  Purification and properties of soluble hydrogenase from the cyanobacterium Anabaena cylindrica. , 1989, Archives of biochemistry and biophysics.

[143]  R. Peterson,et al.  Localization of an uptake hydrogenase in anabaena. , 1978, Plant physiology.

[144]  J. Fontecilla-Camps The active site of Ni-Fe hydrogenases: model chemistry and crystallographic results , 1996, JBIC Journal of Biological Inorganic Chemistry.

[145]  J. Waterbury,et al.  Generic assignments, strain histories, and properties of pure cultures of cyanobacteria , 1979 .

[146]  P. Lindblad,et al.  H2-Uptake and evolution in the unicellular cyanobacterium Chroococcidiopsis thermalis CALU 758 , 2000 .

[147]  Interplay between the Specific Chaperone-Like Proteins HybG and HypC in Maturation of Hydrogenases 1, 2, and 3 from Escherichia coli , 2001, Journal of bacteriology.

[148]  R. Krishna,et al.  Hydrogen production by cyanobacteria : Potential, problems and prospects , 1996 .

[149]  P. Lindblad,et al.  Nostoc PCC 73102 AND H 2 Knowledge, Research, and Biotechnological Challenges , 1998 .

[150]  J. Benemann,et al.  Characterization and partial purification of the reversible hydrogenase of Anabaena cylindrica , 1978 .

[151]  E. Blumwald Regulation of nitrogen fixation in heterocyst-forming cyanobacteria , 2022 .

[152]  D. Horner,et al.  Iron hydrogenases and the evolution of anaerobic eukaryotes. , 2000, Molecular biology and evolution.

[153]  J. Hackstein,et al.  A hydrogenosome with pyruvate formate‐lyase: anaerobic chytrid fungi use an alternative route for pyruvate catabolism , 1999, Molecular microbiology.

[154]  H. Matthijs,et al.  Prochlorophytes: The ‘Other’ Cyanobacteria? , 1994 .

[155]  P. Vignais,et al.  The hydrogenase structural operon in Rhodobacter capsulatus contains a third gene, hupM, necessary for the formation of a physiologically competent hydrogenase , 1991, Molecular microbiology.

[156]  T. Thiel Genetic Analysis of Cyanobacteria , 1994 .

[157]  John R. Benemann,et al.  Feasibility analysis of photobiological hydrogen production , 1997 .

[158]  R. Maier,et al.  Common cis-acting region responsible for transcriptional regulation of Bradyrhizobium japonicum hydrogenase by nickel, oxygen, and hydrogen , 1991, Journal of bacteriology.

[159]  M. Tredici,et al.  The role of hydrogen metabolism in photoheterotrophic cultures of the cyanobacterium Nostoc sp. strain Cc isolated from Cycas circinalis L. , 1990 .

[160]  A. Martel,et al.  Ornithine cycle in Nostoc PCC 73102. Arginase, OCT and arginine deiminase, and the effects of addition of external arginine, ornithine, or citrulline , 1993, Archives of Microbiology.

[161]  W. Stewart Algal physiology and biochemistry , 1975 .

[162]  P. Vignais,et al.  Molecular biology of membrane-bound H2 uptake hydrogenases , 2004, Archives of Microbiology.

[163]  Geoffrey D. Smith,et al.  Soluble hydrogenase of Anabaena cylindrica , 1990 .

[164]  S. Kustu,et al.  The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons , 1990, Cell.

[165]  Sayaka,et al.  Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. , 1996, DNA research : an international journal for rapid publication of reports on genes and genomes.

[166]  T. Fatma,et al.  Cell‐type specificity of the Anabaena fdxN‐element rearrangement requires xisH and xisl , 1997, Molecular microbiology.

[167]  H. Bothe,et al.  The occurrence of the hydrogenase in some blue-green algae , 1978, Archives of Microbiology.

[168]  P. Lindblad,et al.  Cyanobacterial hydogenases and biohydrogen: Present status and future potential , 2001 .

[169]  Angela E. Douglas,et al.  The Biology of Symbiosis , 1992 .

[170]  H. Bothe,et al.  Transcriptional Analysis of Hydrogenase Genes in the Cyanobacteria Anacystis nidulans and Anabaena variabilis Monitored by RT-PCR , 2000, Current Microbiology.

[171]  B. Bergman,et al.  A novel genome rearrangement involved in heterocyst differentiation of the cyanobacterium Anabaena sp. PCC 7120 , 1994 .

[172]  H. Bothe,et al.  Cloning, molecular analysis and insertional mutagenesis of the bidirectional hydrogenase genes from the cyanobacterium Anacystis nidulans , 1996, FEBS letters.

[173]  R. Haselkorn,et al.  Nitrogen fixation (nif) genes of the cyanobacterium Anabaena species strain PCC 7120. The nifB-fdxN-nifS-nifU operon. , 1989, The Journal of biological chemistry.

[174]  D Madamwar,et al.  Ultrastructure of the fresh water cyanobacterium Anabaena variabilis SPU 003 and its application for oxygen-free hydrogen production. , 2001, FEMS microbiology letters.

[175]  C. Wolk,et al.  Heterocyst formation. , 1996, Annual review of genetics.

[176]  R. Maier,et al.  The sequences of hypF, hypC and hypD complete the hyp gene cluster required for hydrogenase activity in Bradyrhizobium japonicum. , 1997, Gene.

[177]  G. Roberts,et al.  Biological nitrogen fixation. , 1993, Annual review of nutrition.

[178]  Possible evolutionary relationship between mammalian alanine:glyoxylate aminotransferase 1 and the 42-kD subunit of cyanobacterial soluble hydrogenase. , 1993, Molecular biology and evolution.

[179]  S. Tabata,et al.  LESSONS FROM SEQUENCING OF THE GENOME OF A UNICELLULAR CYANOBACTERIUM, SYNECHOCYSTIS SP. PCC6803. , 1998, Annual review of plant physiology and plant molecular biology.

[180]  T. Thiel,et al.  Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis , 1997, Journal of bacteriology.

[181]  J. Gallon,et al.  N2 Fixation by non-heterocystous cyanobacteria , 1997 .

[182]  P. J. Johnson,et al.  Molecular analysis of the hydrogenosomal ferredoxin of the anaerobic protist Trichomonas vaginalis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[183]  Photobiological hydrogen production and nitrogenase activity in some heterocystous cyanobacteria , 2001 .

[184]  G. Peschek Evidence for two functionally distinct hydrogenases in Anacystis nidulans , 1979, Archives of Microbiology.

[185]  M Stephenson,et al.  Hydrogenase: a bacterial enzyme activating molecular hydrogen: The properties of the enzyme. , 1931, The Biochemical journal.

[186]  Electron pathways involved in H(2)-metabolism in the green alga Scenedesmus obliquus. , 2001, Biochimica et biophysica acta.

[187]  Lucas J. Stal,et al.  Cyanobacterial Mats and Stromatolites , 2000 .

[188]  Cloning and characterisation of a hyp gene cluster in the filamentous cyanobacterium Nostoc sp. strain PCC 73102. , 2001, FEMS microbiology letters.

[189]  E. Duin,et al.  Infrared-detectable groups sense changes in charge density on the nickel center in hydrogenase from Chromatium vinosum. , 1995, Biochemistry.

[190]  O. Lenz,et al.  A novel multicomponent regulatory system mediates H2 sensing in Alcaligenes eutrophus. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[191]  P. Lindblad,et al.  Hydrogen uptake in Nostoc sp. strain PCC 73102. Cloning and characterization of a hupSL homologue , 1998, Archives of Microbiology.

[192]  B. Bergman,et al.  Immunogold localization of hydrogenase in the cyanobacterial-plant symbioses Peltigera canina, Anthoceros punctatus and Gunnera magellanica , 1992 .

[193]  K. Anagnostidis,et al.  Modern approach to the classification system of cyanophytes. 3 - Oscillatoriales , 1988 .

[194]  R. Gherna Catalogue of strains , 1978 .

[195]  J. Walker,et al.  Mitochondrial NADH:ubiquinone reductase: complementary DNA sequence of the import precursor of the bovine 75-kDa subunit. , 1989, Biochemistry.

[196]  J. William Schopf,et al.  The Fossil Record: Tracing the Roots of the Cyanobacterial Lineage , 2000 .

[197]  M. Medina,et al.  Reversible hydrogenase of Anabaena variabilis ATCC 29413: catalytic properties and characterization of redox centres , 1996, FEBS letters.

[198]  A. Tsygankov,et al.  Reversible hydrogenase activity of Gloeocapsa alpicola in continuous culture , 1998 .

[199]  R. Maier,et al.  Sequences and characterization of hupU and hupV genes of Bradyrhizobium japonicum encoding a possible nickel-sensing complex involved in hydrogenase expression , 1994, Journal of bacteriology.

[200]  H. D. Peck,et al.  Carboxy‐terminal processing of the large subunit of [NiFe] hydrogenases , 1993, FEBS letters.

[201]  R. Maier,et al.  The HypB protein from Bradyrhizobium japonicum can store nickel and is required for the nickel‐dependent transcriptional regulation of hydrogenase , 1997, Molecular microbiology.

[202]  C. P. Whitman,et al.  Chemical and enzymic ketonization of 2-hydroxymuconate, a conjugated enol , 1991 .

[203]  R. O. Morris,et al.  Nucleotide sequence of the genetic loci encoding subunits of Bradyrhizobium japonicum uptake hydrogenase. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[204]  R. Cammack Bioinorganic chemistry: Hydrogenase sophistication , 1999, Nature.

[205]  E. Triplett,et al.  Toward More Productive, Efficient, and Competitive Nitrogen-Fixing Symbiotic Bacteria , 1996 .

[206]  P. Lindblad,et al.  hupS and hupL constitute a transcription unit in the cyanobacterium Nostoc sp. PCC 73102 , 2000, Archives of Microbiology.

[207]  D. Hall,et al.  Hydrogen production by Anabaena variabilis PK84 under simulated outdoor conditions. , 2000, Biotechnology and bioengineering.

[208]  P. Lindblad,et al.  Hydrogen, uptake in Nostoc strain PCC 73102 : effects of nickel, hydrogen, carbon and nitrogen , 1995 .

[209]  T. Happe,et al.  Transcriptional and Mutational Analysis of the Uptake Hydrogenase of the Filamentous CyanobacteriumAnabaena variabilis ATCC 29413 , 2000, Journal of bacteriology.

[210]  Brian A. Whitton,et al.  The Ecology of Cyanobacteria , 2002, Springer Netherlands.