Skip to main content

Nitrogenases and Hydrogenases in Cyanobacteria

  • Chapter
  • First Online:

Abstract

Cyanobacteria may contain different types of nitrogenases that catalyzes (di)nitrogen fixation: two types of Mo-nitrogenases and the V-enzyme. The formation of ammonia by nitrogenases is accompanied with the production of hydrogen gas. This H2-formation is barely detectable in intact cyanobacteria, since the gas is immediately recycled by hydrogenase. Cyanobacteria contain two types of Ni-containing hydrogenases that are defined by their physiological function: An uptake hydrogenase serves to recycle H2, whereas a bidirectional, reversible enzyme catalyzes both uptake and evolution of the gas. The physiological, biochemical and genetic properties of nitrogenases and hydrogenases are described and discussed in this chapter. The constitutive expression of both hydrogenases even under aerobic growth conditions remains puzzling, although suggested explanations for this will be offered. Cyanobacteria are discussed as potential agents for the conversion of solar energy to generate H2-gas for commercial use. Current potentialities will be described at the end of this chapter.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Ananyev G, Carrieri D and Dismukes CG (2008) Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the cyanobacterium Arthospira (Spirulina) maxima. Appl Environ Microbiol 74: 6102–6113

    Article  PubMed  CAS  Google Scholar 

  • Appel J and Schulz R (1998) Hydrogen metabolism in organisms with oxygenic photosynthesis: Hydrogenase as important regulatory devices for a proper redox poising? J Photochem Photobiol Biol 47: 1–11

    Article  CAS  Google Scholar 

  • Appel JSP, Steinmüller K and Schulz R (2000) The bidirectional hydrogenase of Synechocystis PCC 6803 works as an electron valve during photosynthesis. Arch Microbiol 173: 333–338

    Article  PubMed  CAS  Google Scholar 

  • Arnold W, Rump A, Klipp W, Priefer UB and Pühler A (1988) Nucleotide sequence of a 24,206-base-pair DNA fragment carrying the entire nitrogen fixation gene cluster of Klebsiella pneumoniae. J Mol Biol 203: 715–738

    Article  PubMed  CAS  Google Scholar 

  • Asada Y, Koike Y, Schnackenberg J, Miyake M, Uemura I and Miyake J (2000) Heterologous expression of clostridial hydrogenase in the cyanobacterium Synechococcus PCC7942. Bioch Biophys Acta 1490: 269–278

    Article  CAS  Google Scholar 

  • Bauer CC, Scappino L and Haselkorn R (1993) Growth of the cyanobacterium Anabaena on molecular nitrogen: NifJ is required when iron is limited. Proc Natl Acad Sci U S A 90: 8812–8816

    Article  PubMed  CAS  Google Scholar 

  • Benemann JR and Weare NM (1974) Hydrogen evolution by nitrogen fixing Anabaena cylindrical cultures. Science 129: 174–175

    Article  Google Scholar 

  • Betancourt DA, Loveless TM, Brown J and Bishop PE (2008) Characterization of diazotrophs containing Mo-independent nitrogenases, isolated from diverse natural environments. Appl Environ Microbiol 74: 3471–3480

    Article  PubMed  CAS  Google Scholar 

  • Bishop P and Joerger RD (1990) Genetics and molecular biology of alternative nitrogen fixing systems. Ann Rev Plant Physiol Plant Mol Biol 41: 109–125

    Article  CAS  Google Scholar 

  • Böck A, King PW, Blokesch M and Posewitz MC (2006) Maturation of hydrogenases. Adv Microbiol Physiol 51: 1–71

    Article  Google Scholar 

  • Boison G, Schmitz O, Schmitz B and 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

    Article  PubMed  CAS  Google Scholar 

  • Boison G, Bothe H and Schmitz O (2000) Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR. Curr Microbiol 40: 315–321

    Article  PubMed  CAS  Google Scholar 

  • Boison G, Mergel A, Jolkver H and Bothe H (2004) Bacterial life and dinitrogen fixation at a gypsum rock. Appl Environ Microbiol 70: 7070–7077

    Article  PubMed  CAS  Google Scholar 

  • Boison G, Steingen C, Stal LJ and Bothe H (2006) The rice field cyanobacteria Anabaena azotica and Anabaena sp.CH1 express vanadium-dependent nitrogenase. Archiv Microbiol 186: 367–376

    Article  CAS  Google Scholar 

  • Bothe H (1969) Ferredoxin als Kofaktor der cylischen Photophosphorylierung in einem zellfreien System aus der Blaualge Anacystis nidulans. Z Naturforsch 24b: 1574–1582

    Google Scholar 

  • Bothe H and Eisbrenner G (1977) Effect of 7-azatryptophan on nitrogen fixation and heterocyst formation in the blue-green alga Anabaena cylindrica. Biochem Physiol Pflanz 133: 323–332

    Google Scholar 

  • Bothe H and Neuer G (1988) Electron donation to nitrogenase in heterocysts. Methods Enzym 167: 496–501

    Article  CAS  Google Scholar 

  • Bothe H, Distler E and Eisbrenner G (1978) Hydrogen metabolism in blue-green algae. Biochimie 60: 277–289

    Article  PubMed  CAS  Google Scholar 

  • Bothe H, Winkelmann S and Boison G (2008) Maximizing hydrogen production by cyanobacteria. Z Naturforsch 63c: 226–232

    Google Scholar 

  • Carrasco CD, Holliday SD, Hansel A, Lindblad P and Golden JW (2005) Heterocyst-specific excision of the Anabaena strain PCC 7120 hupL element requires xisC. J Bacteriol 187: 6031–6038

    Article  PubMed  CAS  Google Scholar 

  • Chien YT, Auerbruch V, Brabban AD and Zinder SH (2000) Analysis of genes encoding an alternative nitrogenase in the archaeon Methanosarcina barkeri 227. J Bacteriol 182: 3247–3253

    Article  PubMed  CAS  Google Scholar 

  • Cockell CS, Schuerger AC, Billi D, Friedmann EI and Panitz C (2005) Effects of a simulated martian UV flux on the cyanobacterium, Chroococcidiopsis sp. 029. Astrobiol 5: 127–140

    Article  CAS  Google Scholar 

  • Cournac L, Guedeney G, Peltier G and Vignais PM (2004) Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp strain PCC 6803 deficient in the type I NADH-dehydrogenase complex. J Bacteriol 186: 1737–1746

    Article  PubMed  CAS  Google Scholar 

  • Dixon ROD (1972) Hydrogenase in legume root nodule bacteroids, occurrence and properties. Archiv Microbiol 85: 193–201

    CAS  Google Scholar 

  • Eady RR (1996) Structure-function relationship of alternative nitrogenase. Chem Rev 96: 3013–3030

    Article  PubMed  CAS  Google Scholar 

  • Eilmus S, Rösch C and Bothe H (2007) Prokaryotic life in a potash-polluted marsh with emphasis on N-metabolizing microorganisms. Environ Poll 146: 478–491

    Article  CAS  Google Scholar 

  • Ernst A, Reich S and Böger P (1990) Modification of dinitrogen reductase in the cyanobacterium Anabaena variabilis due to C-starvation and ammonia. J Bacteriol 172: 748–755

    PubMed  CAS  Google Scholar 

  • Fewer D, Friedl T and Büdel B (2002) Chroococcidiopsis and heterocysts-differentiating cyanobacteria are each other’s closest living relatives. Mol Phylogenet Evol 23: 82–90

    Article  PubMed  CAS  Google Scholar 

  • Fisher K, Lowe, DJ, Tavares P, Pereira AS, Hynh BH, Edmondson D and Newton WE (2007) Conformations generated during turnover of the Azotobacter vinelandii MoFe protein and their relationship to physiological function. J Inorg Biochem 101: 1649–1656

    Article  PubMed  CAS  Google Scholar 

  • Floener L and Bothe H (1980) Nitrogen fixation in Rhopalodia gibba, a diatom containing blue-greenish inclusions symbiotically. In: Schwemmler W, Schenk HEA (eds) Endocytobiology, Endosymbiosis and Cell Biology, pp 541–552, Walter de Gruyter & Co, Berlin

    Google Scholar 

  • Flores E, Herrero A, Wolk CP and Maldener I (2006) Is the periplasm continuous in filamentous cyanobacteria? Trends Microbiol 14: 439–443

    Article  PubMed  CAS  Google Scholar 

  • Friedrich B and Schwartz E (1993) Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu Rev Microbiol 47: 351–383

    Article  PubMed  CAS  Google Scholar 

  • Gallon JR (2001) N2 fixation in phototrophs. Adaptation to a specialized way of life. Plant Soil 239: 39–48

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Giddings JW and Staehelin LA (1978) Plasma membrane architecture of Anabaena cylindrica: occurrence of microplasmodesmata and changes associated with heterocyst development and the cell cycle. Eur J Cell Biol 16: 235–249

    Google Scholar 

  • Golden JW and Yoon HS (2003) Heterocyst development in Anabaena. Curr Opin Microbiol 6: 557–563

    Article  PubMed  CAS  Google Scholar 

  • Gutekunst K, Phunpruch S, Schwarz C, Schuchardt S, Schulz-Friedrich R and Appel J (2005) LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. Mol Microbiol 58: 810–823

    Article  PubMed  CAS  Google Scholar 

  • Hall DO, Markov SA, Watanabe Y and Rao KK (1995) The potential applications of cyanobacterial photosythesis for clean technologies. Photosynth Res 46: 159–167

    Article  CAS  Google Scholar 

  • Happe T, Schütz K and Böhme H (2000b) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182: 1624–1631

    Article  CAS  Google Scholar 

  • Haselkorn R (2005) Heterocyst differentiation and nitrogen fixation in Anabaena. In: Wang YP, Lin M, Tian ZX, Elmerich C and Newton WE (eds) Biological nitrogen fixation, sustainable agriculture and the environment, Proceedings of the fourteenth international nitrogen fixation congress, pp 65–68, Springer, Dordrecht

    Chapter  Google Scholar 

  • Henson BJ, Pennington LE, Watson LE and Barnum SR (2008) Excision of the nifD element in heterocystous cyanobacteria. Arch Microbiol 189: 357–366

    Article  PubMed  CAS  Google Scholar 

  • Holmqvist M, Stensjö K, Oliveira P, Lindberg P and Lindblad P (2009) Characterization of the hupLS promoter activity in Nostoc punctiforme ATCC 29133. BMC Microbiol 9:54

    Article  PubMed  Google Scholar 

  • Houchins JP (1984) The physiology and biochemistry of hydrogen metabolism in cyanobacteria. Biochim Biophys Acta 768: 227–255

    Article  CAS  Google Scholar 

  • Ihara M (2006a) Light-driven production by a hybrid complex of a [NiFe]-Hydrogenase and the cyanobacterial photosystem I. Photochem Photobiol 82: 676–682

    Article  CAS  Google Scholar 

  • Ihara M, Nakamoto H, Kamachi T, Okura I and Maeda M (2006b) Light-driven hydrogen production by a hybrid complex of a [NiFe]-hydrogenase and the cyanobacterial photosystem I. Photochem Photobiol 82: 1677–1685

    CAS  Google Scholar 

  • Kentemich T, Danneberg G, Hundeshagen B and Bothe H (1988) Evidence for the occurrence of the alternative, vanadium-containing nitrogenase in the cyanobacterium Anabaena variabilis. FEMS Microbiol Lett 51: 19–24

    Article  CAS  Google Scholar 

  • Kentemich T, Haverkamp G and Bothe H (1991a) The expression of a third nitrogenase in the cyanobacterium Anabaena variabilis. Z Naturforsch 46c: 217–222

    Google Scholar 

  • Kentemich T, Casper M and Bothe H (1991b) The reversible hydrogenase in Anacystis nidulans is a component of the cytoplasmic membrane. Naturwissenschaften 78: 559–560

    Article  CAS  Google Scholar 

  • Kessler PS, McLarnan J and Leigh JA (1997) Nitrogenase phylogeny and the molybdenum dependence of nitrogen fixation in Methanococcus maripaludis. J Bacteriol 179: 541–543

    PubMed  CAS  Google Scholar 

  • Laczkó I (1986) Appearance of a reversible hydrogenase activity in Anabaena cylindrica grown in high light. Physiol Plant 67: 634–637

    Article  Google Scholar 

  • Leach CK and Carr NG (1971) Pyruvate:ferredoxin oxidoreductase and its activation by ATP in the blue-green alga Anabaena variabilis. Biochim Biophys Acta 245: 165–174

    Article  PubMed  CAS  Google Scholar 

  • Lindblad P, Christensson K, Lindberg P, Federov A, Pinto G and Tsygankov A (2002) Photoproduction of H2 by wildtype Anabaena PCC 7120 and a hydrogenase deficient mutant: from laboratory experiments to outdoor culture. Int J Hydrogen Energy 27: 1271–1281

    Article  CAS  Google Scholar 

  • Loveless TM, Saah JR and Bishop PE (1999) Isolation of nitrogen-fixing bacteria containing molybdenum—independent nitrogenases from natural environments. Appl Environ Microbiol 65: 4223–4225

    PubMed  CAS  Google Scholar 

  • Ludwig M, Schulz-Friedrich R and Appel J (2006) Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: implications for the phylogenetic origin of cyanobacterial and algal hydrogenases. J Mol Evol 63: 758–768

    Article  PubMed  CAS  Google Scholar 

  • Madamwar D, Garg N and Shah V (2000) Cyanobacterial hydrogen production. World J Microbiol Biotechnol 16: 757–767

    Article  CAS  Google Scholar 

  • Markov SA, Lichtl R, Bazin MJ and Hall DO (1995) Hydrogen production and carbon dioxide uptake by immobilised Anabaena variabilis in a hollow fibre photobioreactor. Enzyme Microb Biotechnol 17: 306–310

    Article  CAS  Google Scholar 

  • Masepohl B, Scholisch K, Görlitz K, Kiutski C and Böhme H (1997) The heterocyst-specific fdxH gene product of the cyanobacterium Anabaena sp. PCC 7120 is important but not essential for nitrogen fixation. Mol Gen Genet 253: 770–776

    Article  PubMed  CAS  Google Scholar 

  • Masukawa H, Mochimaru M and Sakurai H (2002) Disruption of the uptake hydrogenase gene, but not of the bidirectional hydrogenase gene, leads to enhanced photobiological hydrogen production by the nitrogen-fixing cyanobacterium Anabaena sp. PCC 7120. Appl Microbiol Biotech 58: 618–624

    Article  CAS  Google Scholar 

  • Meeks JC and Elhai J (2002) Regulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66: 94–121

    Article  PubMed  CAS  Google Scholar 

  • Mikheeva LE, Schmitz O, Shestakov SV and Bothe H (1995) Mutants of the cyanobacterium Anabaena variabilis altered in hydrogenase activities. Z Naturforsch 50c: 505–510

    Google Scholar 

  • Mullineaux CW (2008) Mechanisms of intercellular molecule exchange in heterocyst-forming cyanobacteria. Embo J 27: 1299–1308

    Article  PubMed  CAS  Google Scholar 

  • Neuer G and Bothe H (1982) The pyruvate: ferredoxin oxidoreductase in heterocyts of the cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 716: 358–365

    Article  PubMed  CAS  Google Scholar 

  • Newton WE (2007) Physiology, biochemistry, and molecular biology of nitrogen fixation. In: Bothe H, Ferguson SJ and Newton WE (eds), Biology of the nitrogen cycle, pp 109–129. Elsevier, Amsterdam

    Chapter  Google Scholar 

  • Oliveira P and Lindblad P (2005) LexA. A transcriptional regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC6803. FEMS Microbiol Lett 251: 59–66

    Article  PubMed  CAS  Google Scholar 

  • Papen H, Kentemich T, Schmülling T and Bothe H (1986) Hydrogenase activities in cyanobacteria. Biochimie 68: 121–132

    Article  PubMed  CAS  Google Scholar 

  • Pau RN (1991) The alternative nitrogenases. In: Dilworth MJ, Glenn AR (eds) Biology and biochemistry of nitrogen fixation, pp 37–57. Elsevier, Amsterdam

    Google Scholar 

  • Prechtl J, Kneip C, Lockhart P, Wenderoth K and Maier UG (2004) Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol 21: 1477–1481

    Article  PubMed  CAS  Google Scholar 

  • Rösch C and Bothe H (2009) Diversity of total nitrogen-fixing and denitrifying bacteria in an acid forest soil. Eur J Soil Sci 60: 883–894

    Article  Google Scholar 

  • Ruvkun GB and Ausubel FM (1980) Interspecies homology of nitrogenase genes. Proc Natl Acad Sci U S A 77: 191–195

    Article  PubMed  CAS  Google Scholar 

  • Scherer S, Kerfin W and Böger P (1980) Increase of nitrogenase activity in the blue-green alga Nostoc muscorum (cyanobacterium). J Bacteriol 144: 1017–1023

    PubMed  CAS  Google Scholar 

  • Schmitz O, Boison G, Hilscher R, Hundeshagen B, Zimmer W, Lottspeich F and Bothe H (1995) Molecular biological analysis of a directional hydrogenase from cyanobacteria. Eur J Biochem 233: 266–276

    Article  PubMed  CAS  Google Scholar 

  • Schmitz O, Boison G, Salzmann H, Bothe H, Schütz K, Wang S and Happe T (2002) HoxE—a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim Biophys Acta 1554: 66–74

    Article  PubMed  CAS  Google Scholar 

  • Schmitz O, Bothe H (1996) NAD(P)+-dependent hydrogenase activity in extracts from the cyanobacterium Anacystis nidulans. FEMS Microbiol Lett 69: 176–182

    Google Scholar 

  • Schmitz O, Kentemich T, Zimmer W, Hundeshagen B and Bothe H (1993) Identification of the nifJ gene coding for pyruvate: ferredoxin oxidoreductase in dinitrogen-fixing cyanobacteria. Arch Microbiol 160: 62–67

    PubMed  CAS  Google Scholar 

  • Schmitz O, Boison G and Bothe H (2001a) Quantitative analysis of two circadian clock-controlled gene clusters coding for the birectional hydrogenase in the cyanobacterium Synechoccus sp. PCC7942. Mol Microbiol 41: 1409–1417

    Article  CAS  Google Scholar 

  • Schmitz O, Gurke J and Bothe H (2001b) Molecular evidence for the aerobic expression of nifJ, encoding pyruvate: ferredoxin oxidoreductase, in cyanobacteria. FEMS Microbiol Lett 195: 97–102

    Article  CAS  Google Scholar 

  • Schrautemeier B, Neveling U and Schmitz S (1995) Distinct and differentially regulated Mo-dependent nitrogen-fixing systems evolved for heterocysts and vegetative cells of Anabaena variabilis ATCC 29413: characterization of the fdX1/2 gene regions as part of the nif1/2 gene clusters. Mol Microbiol 18: 357–359

    Article  PubMed  CAS  Google Scholar 

  • Schütz K (2004) Cyanobacterial H2-production—a comparative analysis. Planta 218: 350–359

    Article  PubMed  Google Scholar 

  • Shah GR, Karunakaran R and Kumar GN (2007) In vivo restriction endonuclease activity of the Anabaena PCC 7120 XisA protein in Escherichia coli. Res Microbiol 158: 679–684

    Article  PubMed  CAS  Google Scholar 

  • Stal LJ and Mozelaar R (1997) Fermentation in cyanobacteria. FEMS Microb Rev 21: 179–211

    Article  CAS  Google Scholar 

  • Stewart WDP and Lex M (1970) Nitrogenase activity in the blue-green alga Plectonema boryanum. Arch Mikrobiol 73: 250–260

    Article  PubMed  CAS  Google Scholar 

  • Tamagnini P (2007) Cyanobacterial hydrogenases. Diversity, regulation and application. FEMS Microb Rev 31: 692–720

    Article  CAS  Google Scholar 

  • Tamagnini P, Costa J-L, Almeida L, Oliveira M-J, Salema R and Lindblad P (2000) Diversity of cyanobacterial hydrogenases, a molecular approach. Curr Microbiol 40: 356–361

    Article  PubMed  CAS  Google Scholar 

  • Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R and Lindblad P (2002) Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66: 1–20

    Article  PubMed  CAS  Google Scholar 

  • Thiel T (1993) Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. J Bacteriol 175: 6276–6286

    PubMed  CAS  Google Scholar 

  • Thiel T, Lyons EM, Erker J and Ernst A (1995) A second nitrogenase in vegetative cells of a heterocyst-forming cyanobacterium. Proc Natl Acad Sci U S A 92: 9358–9362

    Article  PubMed  CAS  Google Scholar 

  • Thiel T, Lyons EM and Thielemeyer J (1998) Organization and regulation of two clusters of nif genes in the cyanobacterium Anabaena variabilis. In: Peschek GA, Loeffelhardt W, Schmetterer G (eds) Phototrophic Prokaryotes, pp 517–521, Plenum Press, New York

    Google Scholar 

  • Thomas JC, Ughy B, Lagoutte B and Ajlani G (2006) A second isoform of ferredoxin:NADP oxidoreductase generated by an in-frame initiation of translation. Proc Natl Acad Sci U S A 103: 18368–18373

    Article  PubMed  CAS  Google Scholar 

  • Trebst A and Bothe H (1966) Zur Rolle des Phytoflavins im photosynthetischen Elektronentransport. Ber Dtsch Bot Ges 79: 44–47

    CAS  Google Scholar 

  • Tsygankov A (2007) Nitrogen fixing cyanobacteria: a review. Appl Biochem Microbiol 43: 250–259

    Article  CAS  Google Scholar 

  • Van der Oost J, Builthuis BA, Feitz S, Krab K and Kraayenhof R (1989) Fermentation metabolism of the unicellular cyanobacterium Cyanothece PCC 7822. Arch Microbiol 151: 415–419

    Article  Google Scholar 

  • Vignais PM and Billoud B (2007) Occurrence, classification and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272

    Article  PubMed  CAS  Google Scholar 

  • Vignais PM and Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6: 159–188

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Walsby AE (2007) Cyanobacterial heterocysts. Terminal pores proposed as sites of gas exchange. Trends Microbiol 15: 340–349

    Article  PubMed  CAS  Google Scholar 

  • Weyman PD, Pratte B and Thiel T (2008) Transcription of hupSL in Anabaena variabilis ATTC 29143 is regulated by NtcA and not by hydrogen. Appl Environ Microbiol 74: 2103–2110

    Article  PubMed  CAS  Google Scholar 

  • Zehr JP (2008) Globally distributed uncultivated oceanic N2-fxing cyanobacteria lack oxygenic photosystem II. Science 322: 1110–1112

    Article  PubMed  CAS  Google Scholar 

  • Zhao Y, Bian SM, Zhou HN and Huang JF (2006) Diversity of nitrogenase systems in diazotrophs. J Integrative Plant Biol 48: 745–755

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hermann Bothe .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Bothe, H., Schmitz, O., Yates, M.G., Newton, W.E. (2011). Nitrogenases and Hydrogenases in Cyanobacteria. In: Peschek, G., Obinger, C., Renger, G. (eds) Bioenergetic Processes of Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0388-9_6

Download citation

Publish with us

Policies and ethics