Nitrogen Fixation and Hydrogen Metabolism in Cyanobacteria

SUMMARY This review summarizes recent aspects of (di)nitrogen fixation and (di)hydrogen metabolism, with emphasis on cyanobacteria. These organisms possess several types of the enzyme complexes catalyzing N2 fixation and/or H2 formation or oxidation, namely, two Mo nitrogenases, a V nitrogenase, and two hydrogenases. The two cyanobacterial Ni hydrogenases are differentiated as either uptake or bidirectional hydrogenases. The different forms of both the nitrogenases and hydrogenases are encoded by different sets of genes, and their organization on the chromosome can vary from one cyanobacterium to another. Factors regulating the expression of these genes are emerging from recent studies. New ideas on the potential physiological and ecological roles of nitrogenases and hydrogenases are presented. There is a renewed interest in exploiting cyanobacteria in solar energy conversion programs to generate H2 as a source of combustible energy. To enhance the rates of H2 production, the emphasis perhaps needs not to be on more efficient hydrogenases and nitrogenases or on the transfer of foreign enzymes into cyanobacteria. A likely better strategy is to exploit the use of radiant solar energy by the photosynthetic electron transport system to enhance the rates of H2 formation and so improve the chances of utilizing cyanobacteria as a source for the generation of clean energy.

[1]  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.

[2]  G. Bernát,et al.  Towards efficient hydrogen production: the impact of antenna size and external factors on electron transport dynamics in Synechocystis PCC 6803 , 2009, Photosynthesis Research.

[3]  R. Haselkorn,et al.  Heterocyst-Specific Expression of patB, a Gene Required for Nitrogen Fixation in Anabaena sp. Strain PCC 7120 , 2003, Journal of bacteriology.

[4]  P. D. Weyman,et al.  Transcription of hupSL in Anabaena variabilis ATCC 29413 Is Regulated by NtcA and Not by Hydrogen , 2008, Applied and Environmental Microbiology.

[5]  Y. Zhang,et al.  PII Is Important in Regulation of Nitrogen Metabolism but Not Required for Heterocyst Formation in the Cyanobacterium Anabaena sp. PCC 7120* , 2007, Journal of Biological Chemistry.

[6]  H. Bothe,et al.  Effect of 7-Azatryptophan on Nitrogen Fixation and Heterocyst Formation in the Blue-green Alga Anabaena cylindrica , 1977 .

[7]  C. Carrano,et al.  Transition Metals in Microbial Metabolism , 1997 .

[8]  P. Lindblad,et al.  LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. , 2005, FEMS microbiology letters.

[9]  Anne Volbeda,et al.  Introduction of methionines in the gas channel makes [NiFe] hydrogenase aero-tolerant. , 2009, Journal of the American Chemical Society.

[10]  M. Yates Electron transport to nitrogenase in Azotobacter chroococcum: Azotobacter flavodoxin hydroquinone as an electron donor , 1972, FEBS letters.

[11]  M. Maeda,et al.  Photoinduced Hydrogen Production by Direct Electron Transfer from Photosystem I Cross-Linked with Cytochrome c3 to [NiFe]-Hydrogenase , 2006, Photochemistry and photobiology.

[12]  E. Schwartz,et al.  Molecular biology of hydrogen utilization in aerobic chemolithotrophs. , 1993, Annual review of microbiology.

[13]  The Structure of the ADP•AlF4- stabilized nitrogenase complex and its implications for signal transduction mechanism , 1997 .

[14]  Enrique Flores,et al.  Mechanism of intercellular molecular exchange in heterocyst‐forming cyanobacteria , 2008, The EMBO journal.

[15]  Xiaoli Z. Fern,et al.  Optimization of pH and nitrogen for enhanced hydrogen production by Synechocystis sp. PCC 6803 via statistical and machine learning methods , 2009, Biotechnology progress.

[16]  Michael Y. Galperin,et al.  The cyanobacterial genome core and the origin of photosynthesis , 2006, Proceedings of the National Academy of Sciences.

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

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

[19]  P. Lindblad,et al.  Cyanobacterial H2 production — a comparative analysis , 2004, Planta.

[20]  J. van der Oost,et al.  Fermentation metabolism of the unicellular cyanobacterium Cyanothece PCC 7822 , 1989, Archives of Microbiology.

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

[22]  K. Ohki,et al.  Detection of nitrogenase in individual cells of a natural population of trichodesmium using immunocytochemical methods for fluorescent cells , 2009 .

[23]  S. Laurent,et al.  Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals , 2006, Molecular microbiology.

[24]  A. Trebst,et al.  Biology of Inorganic Nitrogen and Sulfur , 1981, Proceedings in Life Sciences.

[25]  H. Bothe,et al.  [52] Electron donation to nitrogenase in heterocysts , 1988 .

[26]  P. Bishop,et al.  Identification of genes unique to Mo-independent nitrogenase systems in diverse diazotrophs. , 1999, Canadian journal of microbiology.

[27]  Kensuke Nakamura,et al.  Survey of the Distribution of Different Types of Nitrogenases and Hydrogenases in Heterocyst-Forming Cyanobactera , 2009, Marine Biotechnology.

[28]  W. Buikema,et al.  The role of HetN in maintenance of the heterocyst pattern in Anabaena sp. PCC 7120 , 2001, Molecular microbiology.

[29]  W. Lubitz,et al.  Purification, crystallization and preliminary X-ray analysis of the membrane-bound [NiFe] hydrogenase from Allochromatium vinosum. , 2008, Acta Crystallographica. Section F : Structural Biology and Crystallization Communications.

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

[31]  D. M. Pederson,et al.  The use of nickel to probe the role of hydrogen metabolism in cyanobacterial nitrogen fixation. , 1986, Biochimie.

[32]  D. Bryant,et al.  Photosystem I/molecular wire/metal nanoparticle bioconjugates for the photocatalytic production of H2. , 2008, Journal of the American Chemical Society.

[33]  G. Schraa,et al.  Anaerobic reduction of ethene to ethane in an enrichment culture , 1998 .

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

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

[36]  J. W. Golden,et al.  The Anabaena sp. Strain PCC 7120 Gene all2874 Encodes a Diguanylate Cyclase and Is Required for Normal Heterocyst Development under High-Light Growth Conditions , 2008, Journal of bacteriology.

[37]  Vladimir Espinosa Angarica,et al.  Cross-talk between iron and nitrogen regulatory networks in anabaena (Nostoc) sp. PCC 7120: identification of overlapping genes in FurA and NtcA regulons. , 2007, Journal of molecular biology.

[38]  Identification of the nifJ gene coding for pyruvate: ferredoxin oxidoreductase in dinitrogen-fixing cyanobacteria , 2004, Archives of Microbiology.

[39]  M. Seibert,et al.  Recombinant and in vitro expression systems for hydrogenases: new frontiers in basic and applied studies for biological and synthetic H2 production. , 2009, Dalton transactions.

[40]  D. Rees,et al.  Nitrogenase MoFe-Protein at 1.16 Å Resolution: A Central Ligand in the FeMo-Cofactor , 2002, Science.

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

[42]  M. Gupta,et al.  Enzyme Activities Related to Cyanophycin Metabolism in Heterocysts and Vegetative Cells of Anabaena spp. , 1981 .

[43]  J. Meeks,et al.  Formation of glutamine from [13n]ammonia, [13n]dinitrogen, and [14C]glutamate by heterocysts isolated from Anabaena cylindrica , 1977, Journal of bacteriology.

[44]  E. Padan,et al.  Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria , 1977, Journal of bacteriology.

[45]  J. Zehr,et al.  Characterization of diatom-cyanobacteria symbioses on the basis of nifH, hetR and 16S rRNA sequences. , 2006, Environmental microbiology.

[46]  B. Bergman,et al.  Expression of cyanobacterial genes involved in heterocyst differentiation and dinitrogen fixation along a plant symbiosis development profile. , 2004, Molecular plant-microbe interactions : MPMI.

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

[48]  R. Haselkorn Heterocyst Differentiation and Nitrogen Fixation in Anabaena , 2005 .

[49]  H. Bothe,et al.  The reversible hydrogenase inAnacystis nidulans is a component of the cytoplasmic membrane , 1991, Naturwissenschaften.

[50]  J. Appel,et al.  Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. , 2007, Biochimica et biophysica acta.

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

[52]  L. Seefeldt,et al.  Substrate interactions with nitrogenase: Fe versus Mo. , 2004, Biochemistry.

[53]  M. Ludwig,et al.  Occurrence of Hydrogenases in Cyanobacteria and Anoxygenic Photosynthetic Bacteria: Implications for the Phylogenetic Origin of Cyanobacterial and Algal Hydrogenases , 2006, Journal of Molecular Evolution.

[54]  B. Brito,et al.  Host-dependent expression of Rhizobium leguminosarum bv. viciae hydrogenase is controlled at transcriptional and post-transcriptional levels in legume nodules. , 2008, Molecular plant-microbe interactions : MPMI.

[55]  L. Gèitler Zur Entwicklungsgeschichte der EpithemiaceenEpithemia, Rhopalodia undDenticula (Diatomophyceae) und ihre vermutlich symbiotischen Sphäroidkörper , 1977, Plant Systematics and Evolution.

[56]  P. Lindblad,et al.  Transcriptional Regulation of Nostoc Hydrogenases: Effects of Oxygen, Hydrogen, and Nickel , 2002, Applied and Environmental Microbiology.

[57]  F. B. Simpson,et al.  Hydrogen-stimulated CO2 fixation and coordinate induction of hydrogenase and ribulosebiphosphate carboxylase in a H2-uptake positive strain of Rhizobium japonicum , 1979, Archives of Microbiology.

[58]  Paulette M. Vignais,et al.  Sustained Photoevolution of Molecular Hydrogen in a Mutant of Synechocystis sp. Strain PCC 6803 Deficient in the Type I NADPH-Dehydrogenase Complex , 2004, Journal of bacteriology.

[59]  P. Bisen,et al.  Nutritional and therapeutic potential of Spirulina. , 2005, Current pharmaceutical biotechnology.

[60]  C. Rösch,et al.  Diversity of total, nitrogen‐fixing and denitrifying bacteria in an acid forest soil , 2009 .

[61]  J. Leigh,et al.  Nitrogenase phylogeny and the molybdenum dependence of nitrogen fixation in Methanococcus maripaludis , 1997, Journal of bacteriology.

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

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

[64]  Michael Seibert,et al.  Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. , 2007, Annual review of plant biology.

[65]  B. Büdel,et al.  Chroococcidiopsis and heterocyst-differentiating cyanobacteria are each other's closest living relatives. , 2002, Molecular phylogenetics and evolution.

[66]  A. Tsygankov Nitrogen-fixing cyanobacteria: A review , 2007, Applied Biochemistry and Microbiology.

[67]  W. Martin,et al.  Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. , 2008, Molecular biology and evolution.

[68]  Peter Lindblad,et al.  An AbrB-Like Protein Regulates the Expression of the Bidirectional Hydrogenase in Synechocystis sp. Strain PCC 6803 , 2007, Journal of bacteriology.

[69]  A. Muro-Pastor,et al.  HetR-Dependent and -Independent Expression of Heterocyst-Related Genes in an Anabaena Strain Overproducing the NtcA Transcription Factor , 2005, Journal of bacteriology.

[70]  W. Newton Physiology, Biochemistry, and Molecular Biology of Nitrogen Fixation , 2007 .

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

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

[73]  B. Díez,et al.  Marine diazotrophic cyanobacteria: Out of the blue , 2008 .

[74]  W. Vermaas,et al.  Succinate:Quinol Oxidoreductases in the Cyanobacterium Synechocystis sp. Strain PCC 6803: Presence and Function in Metabolism and Electron Transport , 2000, Journal of bacteriology.

[75]  D. Bryant,et al.  Wiring photosystem I for direct solar hydrogen production. , 2010, Biochemistry.

[76]  J. Bantle,et al.  Estimation of gene expression in heterocysts of Anabaena variabilis by using DNA-RNA hybridization , 1986, Journal of bacteriology.

[77]  Shigeki Ehira,et al.  NrrA Directly Regulates Expression of hetR during Heterocyst Differentiation in the Cyanobacterium Anabaena sp. Strain PCC 7120 , 2006, Journal of bacteriology.

[78]  L. E. Mikheeva,et al.  Genetic control of hydrogen metabolism in cyanobacteria , 2006, Russian Journal of Genetics.

[79]  G. Voordouw,et al.  Effects of Deletion of Genes Encoding Fe-Only Hydrogenase of Desulfovibrio vulgaris Hildenborough on Hydrogen and Lactate Metabolism , 2002, Journal of bacteriology.

[80]  Richard Willstätter,et al.  Untersuchungen über die Assimilation der Kohlensäure: Sieben Abhandlungen , 1918 .

[81]  H. Sakurai,et al.  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 , 2002, Applied Microbiology and Biotechnology.

[82]  O. Lenz,et al.  Light-driven Hydrogen Production by a Hybrid Complex of a [NiFe]-Hydrogenase and the Cyanobacterial Photosystem I , 2006, Photochemistry and photobiology.

[83]  T. Antal,et al.  Production of H2 by sulphur‐deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH , 2005, Journal of applied microbiology.

[84]  E. Flores,et al.  Transcription Activation by NtcA and 2-Oxoglutarate of Three Genes Involved in Heterocyst Differentiation in the Cyanobacterium Anabaena sp. Strain PCC 7120 , 2008, Journal of bacteriology.

[85]  J. W. Golden,et al.  Different functions of HetR, a master regulator of heterocyst differentiation in Anabaena sp. PCC 7120, can be separated by mutation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[86]  U. Eberhardt,et al.  Regulatory Phenomena in the Metabolism of Knallgasbacteria , 1972 .

[87]  Paula Tamagnini,et al.  Hydrogenases and Hydrogen Metabolism of Cyanobacteria , 2002, Microbiology and Molecular Biology Reviews.

[88]  J. Meeks,et al.  Regulation of Cellular Differentiation in Filamentous Cyanobacteria in Free-Living and Plant-Associated Symbiotic Growth States , 2002, Microbiology and Molecular Biology Reviews.

[89]  A. Melis,et al.  Hydrogen production. Green algae as a source of energy. , 2001, Plant physiology.

[90]  R. Haselkorn Developmentally regulated gene rearrangements in prokaryotes. , 1992, Annual review of genetics.

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

[92]  Robert H. White,et al.  The genome of M. acetivorans reveals extensive metabolic and physiological diversity. , 2002, Genome research.

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

[94]  James W. Brown,et al.  Characterization of Diazotrophs Containing Mo-Independent Nitrogenases, Isolated from Diverse Natural Environments , 2008, Applied and Environmental Microbiology.

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

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

[97]  R. Dixon,et al.  Hydrogenase in legume root nodule bacteroids: Occurrence and properties , 2004, Archiv für Mikrobiologie.

[98]  Ludwig Eichinger,et al.  Large scale multiplex PCR improves pathogen detection by DNA microarrays , 2009, BMC Microbiology.

[99]  A. Mergel,et al.  Bacterial Life and Dinitrogen Fixation at a Gypsum Rock , 2004, Applied and Environmental Microbiology.

[100]  S. Shima,et al.  The exchange activities of [Fe] hydrogenase (iron–sulfur-cluster-free hydrogenase) from methanogenic archaea in comparison with the exchange activities of [FeFe] and [NiFe] hydrogenases , 2007, JBIC Journal of Biological Inorganic Chemistry.

[101]  F. Florencio,et al.  Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[102]  K. Furuya,et al.  Latitudinal distribution of diazotrophs and their nitrogen fixation in the tropical and subtropical western North Pacific , 2009 .

[103]  P. Lindblad,et al.  Bmc Microbiology Characterization of the Hupsl Promoter Activity in Nostoc Punctiforme Atcc 29133 , 2022 .

[104]  H. Dekker,et al.  From phosphatases to vanadium peroxidases: a similar architecture of the active site. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[105]  H. Bothe,et al.  Quantitative analysis of expression of two circadian clock‐controlled gene clusters coding for the bidirectional hydrogenase in the cyanobacterium Synechococcus sp. PCC7942 , 2001, Molecular microbiology.

[106]  B. Schink Isolation of a hydrogenase-cytochrome b complex from cytoplasmic membranes of Xanthobacter autotrophicus GZ 29 , 1982 .

[107]  D. Hall,et al.  Hydrogen photoproduction and carbon dioxide uptake by immobilized Anabaena variabilis in a hollow-fiber photobioreactor , 1995 .

[108]  H. Bothe Ferredoxin als Kofaktor der cyclischen Photophosphorylierung in einem zellfreien System aus der Blaualge Anacystis nidulans , 1969, Zeitschrift fur Naturforschung. Teil B, Chemie, Biochemie, Biophysik, Biologie und verwandte Gebiete.

[109]  D. Rees,et al.  Structural Basis of Biological Nitrogen Fixation. , 1996, Chemical reviews.

[110]  Rui Seabra,et al.  Immunolocalization of the uptake hydrogenase in the marine cyanobacterium Lyngbya majuscula CCAP 1446/4 and two Nostoc strains. , 2009, FEMS microbiology letters.

[111]  L. Stal,et al.  THE RELATION BETWEEN N2 FIXATION AND H2 METABOLISM IN THE MARINE FILAMENTOUS NONHETEROCYSTOUS CYANOBACTERIUM LYNGBYA AESTUARII CCY 9616 1 , 2009, Journal of phycology.

[112]  L. Geitler On the life history of theEpithemiaceae Epithemia, Rhopalodia andDenticula (Diatomophyceae) and their presumably symbiotic sphaeroid bodies , 1977 .

[113]  A. Walsby Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. , 2007, Trends in microbiology.

[114]  M. Hagemann,et al.  Flavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt‐stressed cells of Synechocystis sp. strain PCC 6803 , 1999 .

[115]  P. Vignais,et al.  Molecular biology of microbial hydrogenases. , 2004, Current issues in molecular biology.

[116]  Röbbe Wünschiers,et al.  Presence and expression of hydrogenase specific C-terminal endopeptidases in cyanobacteria , 2003, BMC Microbiology.

[117]  F. Pinto,et al.  Transcription profiles of hydrogenases related genes in the cyanobacterium Lyngbya majuscula CCAP 1446/4 , 2009, BMC Microbiology.

[118]  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.

[119]  G. Cohen-bazire,et al.  Phototrophic prokaryotes: the cyanobacteria. , 1977, Annual review of microbiology.

[120]  D. Rees,et al.  Structure of ADP·AIF4 –-stabilized nitrogenase complex and its implications for signal transduction , 1997, Nature.

[121]  G. Owttrim,et al.  A Synechocystis LexA‐orthologue binds direct repeats in target genes , 2008, FEBS letters.

[122]  Wei-fei Song,et al.  Characteristics of hydrogen production by immobilized cyanobacterium Microcystis aeruginosa through cycles of photosynthesis and anaerobic incubation , 2009 .

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

[124]  P. Vignais,et al.  Occurrence, classification, and biological function of hydrogenases: an overview. , 2007, Chemical reviews.

[125]  P. Lindblad,et al.  Diversity and transcription of proteases involved in the maturation of hydrogenases in Nostoc punctiforme ATCC 29133 and Nostoc sp. strain PCC 7120 , 2009, BMC Microbiology.

[126]  H. Bothe,et al.  Electron donation to nitrogenase in heterocysts of cyanobacteria , 1985, Archives of Microbiology.

[127]  Frank W. R. Chaplen,et al.  Optimization of media nutrient composition for increased photofermentative hydrogen production by Synechocystis sp. PCC 6803 , 2008 .

[128]  Jizhong Zhou,et al.  Functional Genomic Analysis of Three Nitrogenase Isozymes in the Photosynthetic Bacterium Rhodopseudomonas palustris , 2005, Journal of bacteriology.

[129]  L. Packer,et al.  An inducible hydrogenase in cyanobacteria enhances N2 fixation , 1977, FEBS letters.

[130]  In vivo restriction endonuclease activity of the Anabaena PCC 7120 XisA protein in Escherichia coli. , 2007, Research in microbiology.

[131]  Eva-Mari Aro,et al.  Cyanobacterial NDH-1 complexes: multiplicity in function and subunit composition. , 2007, Physiologia plantarum.

[132]  P. Böger,et al.  Hydrogen metabolism of the unicellular cyanobacterium Chroococcidiopsis thermalis ATCC29380 , 1988 .

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

[134]  J. Noirel,et al.  Quantitative overview of N2 fixation in Nostoc punctiforme ATCC 29133 through cellular enrichments and iTRAQ shotgun proteomics. , 2009, Journal of proteome research.

[135]  T. Happe,et al.  HoxE--a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. , 2002, Biochimica et biophysica acta.

[136]  W. Stewart,et al.  Nitrogenase activity in the blue-green alga Plectonema boryanum strain 594 , 2004, Archiv für Mikrobiologie.

[137]  Ho-Sung Yoon,et al.  Heterocyst development in Anabaena. , 2003, Current opinion in microbiology.

[138]  Brenda S. Pratte,et al.  Cross-Functionality of Nitrogenase Components NifH1 and VnfH in Anabaena variabilis , 2006, Journal of bacteriology.

[139]  C. Rösch,et al.  Prokaryotic life in a potash-polluted marsh with emphasis on N-metabolizing microorganisms. , 2007, Environmental pollution.

[140]  L. Seefeldt,et al.  The interstitial atom of the nitrogenase FeMo-cofactor: ENDOR and ESEEM evidence that it is not a nitrogen. , 2005, Journal of the American Chemical Society.

[141]  L. Stal Is the distribution of nitrogen-fixing cyanobacteria in the oceans related to temperature? , 2009, Environmental microbiology.

[142]  S. Hill,et al.  Inhibition by acetylene of conventional hydrogenase in nitrogen-fixing bacteria , 1976, Nature.

[143]  L. Stal,et al.  The rice field cyanobacteria Anabaena azotica and Anabaena sp. CH1 express vanadium-dependent nitrogenase , 2006, Archives of Microbiology.

[144]  P. Böger,et al.  Nickel-Dependent Uptake-Hydrogenase Activity in the Blue-Green Alga Anabaena variabilis , 1984 .

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

[146]  E. Flores,et al.  Is the periplasm continuous in filamentous multicellular cyanobacteria? , 2006, Trends in microbiology.

[147]  G. Ananyev,et al.  Optimization of Metabolic Capacity and Flux through Environmental Cues To Maximize Hydrogen Production by the Cyanobacterium “Arthrospira (Spirulina) maxima” , 2008, Applied and Environmental Microbiology.

[148]  Biswanath Chakraborty,et al.  Evidence for the occurrence of an alternative nitrogenase system in Azospirillum brasilense , 1995 .

[149]  P. Lockhart,et al.  Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. , 2004, Molecular biology and evolution.

[150]  G. Maróti,et al.  Cyanobacterial-Type, Heteropentameric, NAD+-Reducing NiFe Hydrogenase in the Purple Sulfur Photosynthetic Bacterium Thiocapsa roseopersicina , 2004, Applied and Environmental Microbiology.

[151]  Hideaki Miyashita,et al.  Some Cyanobacteria Synthesize Semi-amylopectin Type α-Polyglucans Instead of Glycogen , 2005 .

[152]  S. Scherer,et al.  Increase of Nitrogenase Activity in the Blue-Green Alga Nostoc muscorum (Cyanobacterium) , 1980, Journal of bacteriology.

[153]  H. Bothe,et al.  Molecular evidence for the aerobic expression of nifJ, encoding pyruvate:ferredoxin oxidoreductase, in cyanobacteria. , 2001, FEMS microbiology letters.

[154]  Ying Zhao,et al.  Diversity of Nitrogenase Systems in Diazotrophs , 2006 .

[155]  H. Papen,et al.  Physiology, biochemistry, and genetics of the uptake hydrogenase in rhizobia. , 1987, Annual review of microbiology.

[156]  R. Haselkorn,et al.  Growth of the cyanobacterium Anabaena on molecular nitrogen: NifJ is required when iron is limited. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[157]  S. Shima,et al.  The Crystal Structure of [Fe]-Hydrogenase Reveals the Geometry of the Active Site , 2008, Science.

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

[159]  H. Bothe,et al.  The pyruvate: ferredoxin oxidoreductase in heterocysts of the cyanobacterium Anabaena cylindrica. , 1982, Biochimica et biophysica acta.

[160]  R. Haselkorn,et al.  Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[161]  A. Kaminski,et al.  Hydrogenases in green algae: do they save the algae's life and solve our energy problems? , 2002, Trends in plant science.

[162]  Ilana Berman-Frank,et al.  Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. , 2003, Research in microbiology.

[163]  O. Lenz,et al.  Impact of alterations near the [NiFe] active site on the function of the H2 sensor from Ralstonia eutropha , 2007, The FEBS journal.

[164]  T. Happe,et al.  How algae produce hydrogen--news from the photosynthetic hydrogenase. , 2009, Dalton transactions.

[165]  Paula Tamagnini,et al.  Cyanobacterial hydrogenases: diversity, regulation and applications. , 2007, FEMS microbiology reviews.

[166]  A. Muro-Pastor,et al.  Role of Two NtcA-Binding Sites in the Complex ntcA Gene Promoter of the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120 , 2008, Journal of bacteriology.

[167]  P. Lindblad,et al.  Heterocyst-Specific Excision of the Anabaena sp. Strain PCC 7120 hupL Element Requires xisC , 2005, Journal of bacteriology.

[168]  C. K. Leach,et al.  Pyruvate: ferredoxin oxidoreductase and its activation by ATP in the blue-green alga Anabaena variabilis. , 1971, Biochimica et biophysica acta.

[169]  M. Ghirardi,et al.  Photobiological hydrogen-producing systems. , 2009, Chemical Society reviews.

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

[171]  U. Neveling,et al.  Distinct and differently regulated Mo‐dependent nitrogen‐fixing systems evolved for heterocysts and vegetative cells of Anabaena variabilis ATCC 29413: characterization of the fdxH1/2 gene regions as part of the nif1/2 gene clusters , 1995, Molecular microbiology.

[172]  G. Ruvkun,et al.  Interspecies homology of nitrogenase genes. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[173]  A. Volbeda,et al.  Experimental approaches to kinetics of gas diffusion in hydrogenase , 2008, Proceedings of the National Academy of Sciences.

[174]  Peter Lindblad,et al.  Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. , 2008, Journal of proteome research.

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

[176]  H. Bothe,et al.  The Hydrogenase-Nitrogenase Relationship in Nitrogen-Fixing Organisms , 1981 .

[177]  Richard Willstätter,et al.  Untersuchungen über die assimilation der kohlensäure. , 1915 .

[178]  J. Meyer,et al.  [FeFe] hydrogenases and their evolution: a genomic perspective , 2007, Cellular and Molecular Life Sciences.

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

[180]  Jason Raymond,et al.  The natural history of nitrogen fixation. , 2004, Molecular biology and evolution.

[181]  P. Lindblad,et al.  Transcriptional regulation of the cyanobacterial bidirectional Hox-hydrogenase. , 2009, Dalton transactions.

[182]  K. Fisher,et al.  Conformations generated during turnover of the Azotobacter vinelandii nitrogenase MoFe protein and their relationship to physiological function. , 2007, Journal of inorganic biochemistry.

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

[184]  H. Papen,et al.  Properties of the glyceraldehyde-3-P dehydrogenase in heterocysts and vegetative cells of cyanobacteria , 1986 .

[185]  William E. Newton,et al.  Biology of the nitrogen cycle , 2007 .

[186]  H. Mazur-Marzec,et al.  Do toxic cyanobacteria blooms pose a threat to the Baltic ecosystem , 2009 .

[187]  I. Vass,et al.  Transcriptional regulation of the bidirectional hydrogenase in the cyanobacterium Synechocystis 6803. , 2009, Journal of biotechnology.

[188]  O. Meyer,et al.  N2 Fixation by Streptomyces thermoautotrophicus Involves a Molybdenum-Dinitrogenase and a Manganese-Superoxide Oxidoreductase That Couple N2Reduction to the Oxidation of Superoxide Produced from O2by a Molybdenum-CO Dehydrogenase* , 1997, The Journal of Biological Chemistry.

[189]  J. W. Golden,et al.  Excision of an 11-kilobase-pair DNA element from within the nifD gene in anabaena variabilis heterocysts , 1989, Journal of bacteriology.

[190]  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 .

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

[192]  August Böck,et al.  Maturation of hydrogenases. , 2006, Advances in microbial physiology.

[193]  P. Ludden,et al.  Purification and Characterization of the vnf-encoded Apodinitrogenase from Azotobacter vinelandii(*) , 1996, The Journal of Biological Chemistry.

[194]  P. Bishop,et al.  Isolation of Nitrogen-Fixing Bacteria Containing Molybdenum-Independent Nitrogenases from Natural Environments , 1999, Applied and Environmental Microbiology.

[195]  R. Premakumar,et al.  Mo-independent nitrogenase 3 is advantageous for diazotrophic growth of Azotobacter vinelandii on solid medium containing molybdenum , 1994, Journal of bacteriology.

[196]  Z. Chen,et al.  Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module , 2006, JBIC Journal of Biological Inorganic Chemistry.

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

[198]  H. Bothe,et al.  The diaphorase subunit HoxU of the bidirectional hydrogenase as electron transferring protein in cyanobacterial respiration? , 1996, Naturwissenschaften.

[199]  H. Bothe,et al.  Flavodoxin from Azotobacter vinelandii. , 1972, Archiv fur Mikrobiologie.

[200]  Schwemmler,et al.  Endocytobiology: Endosymbiosis and Cell Biology:a synthesis of recent research ; proceedings of the International Colloquium on Endosymbiosis and Cell Research , 1980 .

[201]  L. Laczkó Appearance of a reversible hydrogenase activity in Anabaena cylindrica grown in high light , 1986 .

[202]  T. Wood,et al.  Inhibition of hydrogen uptake in Escherichia coli by expressing the hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 , 2007, BMC biotechnology.

[203]  P. Bishop,et al.  Genetics and Molecular Biology of Alternative Nitrogen Fixation Systems , 1990 .

[204]  E. Delong,et al.  Low genomic diversity in tropical oceanic N2-fixing cyanobacteria , 2007, Proceedings of the National Academy of Sciences.

[205]  Jindong Zhao,et al.  Regulation of intracellular free calcium concentration during heterocyst differentiation by HetR and NtcA in Anabaena sp. PCC 7120. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[206]  H. Bothe,et al.  Hydrogen metabolism in blue-green algae. , 1978, Biochimie.

[207]  S. Shima,et al.  The crystal structure of C176A mutated [Fe]‐hydrogenase suggests an acyl‐iron ligation in the active site iron complex , 2009, FEBS letters.

[208]  H. Masukawa,et al.  Hydrogenases and photobiological hydrogen production utilizing nitrogenase system in cyanobacteria , 2002 .

[209]  J. Thomas,et al.  A second isoform of the ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation , 2006, Proceedings of the National Academy of Sciences.

[210]  H. Papen,et al.  The isocitrate dehydrogenase from cyanobacteria , 2004, Archives of Microbiology.

[211]  S. Emerson,et al.  Ocean anoxia and the concentrations of molybdenum and vanadium in seawater , 1991 .

[212]  B. Brito,et al.  Biodiversity of uptake hydrogenase systems from legume endosymbiotic bacteria. , 2005, Biochemical Society transactions.

[213]  Ai Ishii,et al.  An AbrB-Like Transcriptional Regulator, Sll0822, Is Essential for the Activation of Nitrogen-Regulated Genes in Synechocystis sp. PCC 68031[W] , 2008, Plant Physiology.

[214]  L. Curatti,et al.  Sucrose is involved in the diazotrophic metabolism of the heterocyst‐forming cyanobacterium Anabaena sp , 2002, FEBS letters.

[215]  A. Khodursky,et al.  Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803 , 2008, BMC Genomics.

[216]  K. Awai,et al.  Identification of the glycosyl transferase required for synthesis of the principal glycolipid characteristic of heterocysts of Anabaena sp. strain PCC 7120. , 2007, FEMS microbiology letters.

[217]  P. Lindblad,et al.  The bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803 , 2006 .

[218]  R. Eady Structure−Function Relationships of Alternative Nitrogenases , 1996 .

[219]  S. Laurent,et al.  An increase in the level of 2-oxoglutarate promotes heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120. , 2003, Microbiology.

[220]  Jianguo Liu,et al.  Light energy conversion into H2 by Anabaena variabilis mutant PK84 dense cultures exposed to nitrogen limitations , 2006 .

[221]  A. Stoll,et al.  Untersuchungen über die assimilation der kohlensäure. Seiben abhandlungen von Richard Willstätter und Arthur Stoll ... , 1918 .

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

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

[224]  M. Dilworth,et al.  Hydrazine is a product of dinitrogen reduction by the vanadium-nitrogenase from Azotobacter chroococcum. , 1991, The Biochemical journal.

[225]  H. Bothe,et al.  NAD( P)+-dependent hydrogenase activity in extracts from the cyanobacterium Anacystis nidulans , 1996 .

[226]  P. Ludden,et al.  Characterization of VNFG, the delta subunit of the vnf-encoded apodinitrogenase from Azotobacter vinelandii. Implications for its role in the formation of functional dinitrogenase 2. , 1997, The Journal of biological chemistry.

[227]  R. Burris,et al.  Interactions among substrates and inhibitors of nitrogenase , 1975, Journal of bacteriology.

[228]  Z. Svirčev,et al.  MICROALGAE AND CYANOBACTERIA: FOOD FOR THOUGHT 1 , 2008, Journal of phycology.

[229]  F. B. Simpson,et al.  A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. , 1984, Science.

[230]  L. Watson,et al.  Excision of the nifD element in the heterocystous cyanobacteria , 2008, Archives of Microbiology.

[231]  E. Padan,et al.  Hydrogen metabolism in the facultative anoxygenic cyanobacteria (blue-green algae) Oscillatoria limnetica and Aphanothece halophytica , 1978, Archives of Microbiology.

[232]  S. Zinder,et al.  Analysis of Genes Encoding an Alternative Nitrogenase in the Archaeon Methanosarcina barkeri227 , 2000, Journal of bacteriology.

[233]  Patricia Amara,et al.  Structure–function relationships of anaerobic gas-processing metalloenzymes , 2009, Nature.

[234]  C. Cockell,et al.  Effects of a simulated martian UV flux on the cyanobacterium, Chroococcidiopsis sp. 029. , 2005, Astrobiology.

[235]  M. Dilworth,et al.  The alternative nitrogenases. , 1991 .

[236]  Peter Lindblad,et al.  Photoproduction of H2 by wildtype Anabaena PCC 7120 and a hydrogen uptake deficient mutant: from laboratory experiments to outdoor culture , 2002 .

[237]  M. Dilworth,et al.  Ethane formation from acetylene as a potential test for vanadium nitrogenase in vivo , 1987, Nature.

[238]  Jonathan P. Zehr,et al.  Globally Distributed Uncultivated Oceanic N2-Fixing Cyanobacteria Lack Oxygenic Photosystem II , 2008, Science.

[239]  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.

[240]  J. Appel,et al.  LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator , 2005, Molecular microbiology.

[241]  J. Zehr,et al.  Quantitative analysis of nifH genes and transcripts from aquatic environments. , 2005, Methods in enzymology.

[242]  R. D,et al.  Nitrogen Fixation in Bacteria and Higher Plants , 1975, Molecular Biology, Biochemistry and Biophysics.

[243]  H. Bothe,et al.  Maximizing Hydrogen Production by Cyanobacteria , 2008, Zeitschrift fur Naturforschung. C, Journal of biosciences.