Fundamentals and Recent Advances in Hydrogen Production and Nitrogen Fixation in Cyanobacteria

  • Namita Khanna
  • Patrícia Raleiras
  • Peter LindbladEmail author
Part of the Developments in Applied Phycology book series (DAPH, volume 6)


There is an urgent need to develop sustainable solutions to convert solar energy into energy carriers used in the society. In addition to solar cells generating electricity, there are several options to generate solar fuels. Native and engineered cyanobacteria have been as model systems to examine, demonstrate, and develop photobiological hydrogen production. In the present contribution the knowledge and understanding of the native systems in cyanobacteria to generate hydrogen, as well as metabolic modulations and genetic engineering to enhance hydrogen production is presented and summarized. Specifically, the recent insight around ferredoxin/flavodoxin as the likely electron donor to the bidirectional Hox-hydrogenase instead of the generally accepted NAD(P)H is highlighted and discussed. In addition, engineering approaches of [NiFe] hydrogenases for optimal catalytic efficiencies and attempts to express high turnover [FeFe] hydrogenase in cyanobacteria that may facilitate the development of strains to reach target levels of hydrogen production in cyanobacteria are detailed. The fundamental advancements achieved in these fields are summarized in this review.


Cyanobacteria Bidirectional hox-hydrogenase Genetic engineering Hydrogen production Hydrogenase Nitrogenase Uptake hydrogenase 



Research in the authors’ laboratory received funding from the Swedish Energy Agency and the Knut and Alice Wallenberg Foundation (project MoSE).


  1. Adams MWW (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020:115–145PubMedCrossRefGoogle Scholar
  2. Adams DG, Carr NG (1989) Control of heterocyst development in the cyanobacterium Anabaena cylindrica. J Gen Microbiol 135:839–849Google Scholar
  3. Ajlani G, Vernotte C (1998) Construction and characterization of a phycobiliprotein-less mutant of Synechocystis sp. PCC 6803. Plant Mol Biol 37:577–580PubMedCrossRefGoogle Scholar
  4. Allakhverdiev SI, Thavasi V, Kreslavski VD, Zharmukhamedov SK, Klimov VV, Ramakrishna S, Los D, Mimuro M, Nishihara H, Carpentier R (2010) Photosynthetic hydrogen production. J Photochem Photobiol C Photochem Rev 11:101–113CrossRefGoogle Scholar
  5. Ananyev G, Carrieri D, Dismukes GC (2008) Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the cyanobacterium “Arthrospira (Spirulina) maxima”. Appl Environ Microbiol 74:6102–6113PubMedPubMedCentralCrossRefGoogle Scholar
  6. Appel J, Schulz R (1996) Sequence analysis of an operon of NAD(P)-reducing nickel hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 gives additional evidence for direct coupling of the enzyme to NADP(H)-dehydrogenase (complex I). Biochim Biophys Acta 1298:141–147PubMedCrossRefGoogle Scholar
  7. Appel J, Phunpruch S, Schulz R (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch Microbiol 173:333–338PubMedCrossRefGoogle Scholar
  8. Axelsson R, Lindblad P (2002) Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel. J Bacteriol 68:444–447Google Scholar
  9. Baebprasert W, Lindblad P, Incharoensakdi A (2010) Response of H2 production and Hox-hydrogenase activity to external factors in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydrogen Energy 35:6611–6616CrossRefGoogle Scholar
  10. Baebprasert W, Jantaro S, Khetkorn W, Lindblad P, Incharoensakdi A (2011) Increased H2 production in the cyanobacterium Synechocystis sp. strain PCC 6803 by redirecting the electron supply via genetic engineering of the nitrate assimilation pathway. Metab Eng 13:610–616PubMedCrossRefGoogle Scholar
  11. Bandyopadhyay A, Stockel J, Min H, Sherman LA, Pakrasi HB (2010) High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat Commun 1:139PubMedCrossRefGoogle Scholar
  12. Benemann JR (1994) Feasibility analysis of photobiological hydrogen production. In: Block DL, Veziroglu TN (eds) Hydrogen energy progress X. Proceedings of 10th world hydrogen energy congress. Miami, Cocoa Beach, pp 931–940Google Scholar
  13. Benemann JR, Weare NM (1974) Hydrogen evolution by nitrogen-fixing Anabaena cylindrica cultures. Science 184:174–175PubMedCrossRefGoogle Scholar
  14. Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154:157–164PubMedCrossRefGoogle Scholar
  15. Bernát G, Waschewski N, Rögner M (2009) Towards efficient hydrogen production: the impact of antenna size and external factors on electron transport dynamics in Synechocystis PCC 6803. Photosynth Res 99:205–216PubMedCrossRefGoogle Scholar
  16. Björn OL, Govindjee (2008) The evolution of photosynthesis and its environmental impact. In: Björn OL (ed) Photobiology: the science of life and light. Springer, New York, pp 255–287CrossRefGoogle Scholar
  17. Böck A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71PubMedCrossRefGoogle Scholar
  18. Böhme H (1987) Regulation of electron flow to nitrogenase in a cell-free system from heterocysts of Anabaena variabilis. Biochim Biophys Acta 891:121–128CrossRefGoogle Scholar
  19. Böhme H, Schrautemeier B (1987) Electron donation to nitrogenase in a cell-free system from heterocysts of Anabaena variabilis. Biochim Biophys Acta 891:1–7CrossRefGoogle Scholar
  20. Boison G, Bothe H, Hansel A, Lindblad P (1999) Evidence against a common use of the diaphorase subunits by the bidirectional hydrogenase and by the respiratory complex I in cyanobacteria. FEMS Microbiol Lett 174:159–165CrossRefGoogle Scholar
  21. Boison G, Bothe H, Schmitz O (2000) Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR. Curr Microbiol 40:315–321PubMedCrossRefGoogle Scholar
  22. Borowitzka MA (2016) Systematics, taxonomy and species names: do they matter? In: Borowitzka MA, Beardall J, Raven JA (eds) The physiology of microalgae. Springer, Dordrecht, pp 655–681Google Scholar
  23. Bothe H, Schmitz O, Yates MG, Newton WE (2010) Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev 74:529–551PubMedPubMedCentralCrossRefGoogle Scholar
  24. Brazzolotto X, Rubach JK, Gaillard J, Gambarelli S, Atta M, Fontecave M (2006) The [Fe-Fe]-hydrogenase maturation protein HydF from Thermotoga maritima is a GTPase with an iron-sulfur cluster. J Biol Chem 281:769–774PubMedCrossRefGoogle Scholar
  25. Broda E, Pesheck GA (1983) Nitrogen fixation as evidence for the reducing nature of the early atmosphere. Biosystems 16:1–8PubMedCrossRefGoogle Scholar
  26. Buikema WJ, Haselkorn R (1991) Characterization of a gene controlling heterocyst differentiation in the cyanobacterium Anabaena 7120. Genes Dev 5:321–330PubMedCrossRefGoogle Scholar
  27. Buikema WJ, Haselkorn R (2001) Expression of the Anabaena hetR gene from a copper-regulated promoter leads to heterocyst differentiation under repressing conditions. Proc Natl Acad Sci U S A 98:2729–2734PubMedPubMedCentralCrossRefGoogle Scholar
  28. Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B (2005) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10:181–196PubMedCrossRefGoogle Scholar
  29. Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96:2983–3011PubMedCrossRefGoogle Scholar
  30. Camsund D, Lindblad P (2014) Engineered transcriptional systems for cyanobacterial biotechnology. Front Bioengy Biotechnol 2:40Google Scholar
  31. Camsund D, Devine E, Holmqvist M, Yohanoun P, Lindblad P, Stensjö K (2011) A HupS-GFP fusion protein demonstrates a heterocyst-specific localization of the uptake hydrogenase in Nostoc punctiforme. FEMS Microbiol Lett 316:152–159PubMedCrossRefGoogle Scholar
  32. Capone DG (1993) Determination of nitrogenase activity in aquatic samples using the acetylene reduction procedure. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 621–631Google Scholar
  33. Carpenter EJ (1983) Nitrogen fixation by marine Oscillatoria (Trichodesmium) in the world’s oceans. In: Carpenter EJ, Capone DG (eds) Nitrogen in the marine environment. Academic, New York, pp 65–103CrossRefGoogle Scholar
  34. Carrasco CD, Ramaswamy KS, Ramasubramanian TS, Golden JW (1994) Anabaena xisF gene encodes a developmentally regulated site-specific recombinase. Genes Dev 8:74–83PubMedCrossRefGoogle Scholar
  35. Carrasco CD, Garcia JS, Golden JW (1998) Programmed DNA rearrangement of a hydrogenase gene during Anabaena heterocyst development. In: Zaborsky OR (ed) BioHydrogen. Springer, New York, pp 203–207Google Scholar
  36. Carrasco CD, Holliday SD, Hansel A, Lindblad P, Golden JW (2005) Heterocyst-specific excision of the Anabaena sp. strain PCC 7120 hupL element requires xisC. J Bacteriol 187:6031–6038PubMedPubMedCentralCrossRefGoogle Scholar
  37. Carrieri D, Momot D, Brasg I, Ananyev G, Lenz O, Bryant D, Dismukes GC (2010) Boosting autofermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl Environ Microbiol 76:6455–6462PubMedPubMedCentralCrossRefGoogle Scholar
  38. Carrieri D, Wawrousek K, Eckert C, Yu J, Maness PC (2011) The role of the bidirectional hydrogenase in cyanobacteria. Bioresour Technol 102:8368–8377PubMedCrossRefGoogle Scholar
  39. Christiansen J, Seefeldt LC, Dean DR (2000) Competitive substrate and inhibitor interactions at the physiologically relevant active site of nitrogenase. J Biol Chem 275:36104–36107PubMedCrossRefGoogle Scholar
  40. Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R (2011) Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H2-oxidizing bacteria. Appl Environ Microbiol 77:6027–6035PubMedPubMedCentralCrossRefGoogle Scholar
  41. Cournac L, Guedeney G, Peltier G, Vignais PM (2004) Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the Type I NADPH-dehydrogenase complex. J Bacteriol 186:1737–1746PubMedPubMedCentralCrossRefGoogle Scholar
  42. Cournac L, De Lacey AL, Volbeda A, Léger C, Burlat B, Champ S, Martin L, Sanganas O, Haumann M, Fernandez VM, Guigliarelli B, Fontecilla-Camps J, Rousset M (2009) Introduction of methionines in the gas channel makes [NiFe] hydrogenase aero-tolerant. J Am Chem Soc 131:10156–10164PubMedCrossRefGoogle Scholar
  43. Daday A, Platz RA, Smith GD (1977) Anaerobic and aerobic hydrogen gas formation by the blue green alga Anabaena cylindrica. Appl Environ Microbiol 34:478–483PubMedPubMedCentralGoogle Scholar
  44. Daday A, Lambert RG, Smith GD (1979) Measurement in vivo of hydrogenase-catalysed hydrogen evolution in the presence of nitrogenase enzyme in cyanobacteria. Biochem J 177:139–144PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dickson DJ (2011) Photobiological hydrogen production from the cyanobacterium Synechocystis sp. PCC 6803 encapsulated in sol-gel processed silica. PhD thesis, Oregon State University, USAGoogle Scholar
  46. Dilworth MJ, Fisher K, Kim CH, Newton WE (1998) Effects on substrate reduction of substitution of histidine-195 by glutamine in the alpha-subunit of the MoFe protein of Azotobacter vinelandii nitrogenase. Biochemistry 37:17495–17505PubMedCrossRefGoogle Scholar
  47. Ducat DC, Sachdeva G, Silver P (2011) Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proc Natl Acad Sci U S A 108:3941–3946PubMedPubMedCentralCrossRefGoogle Scholar
  48. Eady RR (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96:3013–3030PubMedCrossRefGoogle Scholar
  49. Ehira S (2013) Transcriptional regulation of heterocyst differentiation in Anabaena sp. strain PCC 7120. Russ J Plant Physiol 60:443–452CrossRefGoogle Scholar
  50. Ekman M, Ow SY, Holmqvist M, Zhang X, Van Wagenen J, Wright PC, Stensjö K (2011) Metabolic adaptations in a H2 producing heterocyst-forming cyanobacterium: potentials and implications for biological engineering. J Proteome Res 10:1772–1784PubMedCrossRefGoogle Scholar
  51. Fan Q, Huang G, Lechno-Yossef S, Wolk CP, Kaneko T, Tabata S (2005) Clustered genes required for synthesis and deposition of envelope glycolipids in Anabaena sp. strain PCC 7120. Mol Microbiol 58:227–243PubMedCrossRefGoogle Scholar
  52. Flaherty BL, Nieuwerburgh F, Head SR, Golden JW (2011) Directional RNA deep sequencing sheds new light on the transcriptional response of Anabaena sp. strain PCC 7120 to combined-nitrogen deprivation. BMC Genomics 12:332PubMedPubMedCentralCrossRefGoogle Scholar
  53. Flores E, Herrero A (2010) Compartmentalized function through cell differentiation in filamentous cyanobacteria. Nat Rev Microbiol 8:39–50PubMedCrossRefGoogle Scholar
  54. Forzi L, Hellwig P, Thauer RK, Sawers RG (2007) The CO and CN ligands to the active site Fe in [NiFe]-hydrogenase of Escherichia coli have different metabolic origins. FEMS Lett 581:3317–3321Google Scholar
  55. Frias JE, Flores E, Herrero A (1994) Requirement of the regulatory protein NtcA for the expression of nitrogen assimilation and heterocyst development genes in the cyanobacterium Anabaena sp. PCC 7120. Mol Microbiol 14:823–832PubMedCrossRefGoogle Scholar
  56. Fujita Y, Murakami A (1987) Regulation of electron-transport composition in cyanobacterial photosynthetic system—stoichiometry among Photosystem-I and Photosystem-II complexes and their light-harvesting antennae and Cytochrome-b6 Cytochrome-f complex. Plant Cell Physiol 28:1547–1553Google Scholar
  57. Golden JW (1997) Programmed DNA rearrangements in cyanobacteria. In: de Bruijn FJ, Lupski JR, Weinstock G (eds) Bacterial genomes: physical structure and analysis. Chapman and Hall, New York, pp 162–173Google Scholar
  58. Golden JW, Wiest DR (1988) Genome rearrangement and nitrogen fixation in Anabaena blocked by inactivation of xisA gene. Science 242:1421–1423PubMedCrossRefGoogle Scholar
  59. Golden JW, Robinson SJ, Haselkorn R (1985) Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature 314:419–423PubMedCrossRefGoogle Scholar
  60. Golden JW, Carrasco CD, Mulligan ME, Schneider GJ, Haselkorn R (1988) Deletion of a 55-kilobase-pair DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120. J Bacteriol 170:5034–5041PubMedPubMedCentralGoogle Scholar
  61. Goris T, Wait AF, Saggu M, Fritsch J, Heidary N, Stein M, Zebger I, Lendzian F, Armstrong FA, Friedrich B, Lenz O (2011) A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nat Chem Biol 7:310–318PubMedCrossRefGoogle Scholar
  62. Gutekunst K, Phunpruch S, Schwarz C, Schuchardt S, Schultz-Friedrich R, Appel J (2005) LexA regulates the bidrectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol Microbiol 58:810–823PubMedCrossRefGoogle Scholar
  63. Gutekunst K, Chen X, Schreiber K, Kaspar U, Makam S, Appel J (2014) The bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 is reduced by flavodoxin and ferredoxin and is essential under mixotrophic, nitrate-limiting conditions. J Biol Chem 289:1930–1937PubMedPubMedCentralCrossRefGoogle Scholar
  64. Gutthann F, Egert M, Marques A, Appel J (2007) Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767:161–169PubMedCrossRefGoogle Scholar
  65. Hallenbeck PC, Benemann JR (2002) Biological hydrogen production: fundamentals and limiting processes. Int J Hydrogen Energy 27:1185–1193CrossRefGoogle Scholar
  66. Hallenbeck PC, Abo-Hashesh M, Ghosh D (2012) Strategies for improving biological hydrogen production. Bioresour Technol 110:1–9PubMedCrossRefGoogle Scholar
  67. Happe T, Schühme K (2000) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis. J Bacteriol 182:1624–1631PubMedPubMedCentralCrossRefGoogle Scholar
  68. Happe T, Schütz K, Böhme H (2000) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182:1624–1631PubMedPubMedCentralCrossRefGoogle Scholar
  69. Haselkorn R, Buikema WJ (1992) Nitrogen fixation in cyanobacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Springer, New York, pp 166–190Google Scholar
  70. Hebbar PB, Curtis SE (2000) Characterization of devH, a gene encoding a putative DNA binding protein required for heterocyst function in Anabaena sp. strain PCC 7120. J Bacteriol 182:3572–3581PubMedPubMedCentralCrossRefGoogle Scholar
  71. Heidorn T, Camsund D, Huang H-H, Lindberg P, Oliveira P, Stensjö K, Lindblad P (2011) Synthetic biology in cyanobacteria: engineering and analyzing novel functions. Methods Enzymol 497:540–579Google Scholar
  72. Herrero A, Muro-Pastor AM, Valladares A, Flores E (2004) Cellular differentiation and the NtcA transcription factor in filamentous cyanobacteria. FEMS Microbiol Rev 28:469–487PubMedCrossRefGoogle Scholar
  73. Higa KC, Callahan SM (2010) Ectopic expression of hetP can partially bypass the need for hetR in heterocyst differentiation by Anabaena sp. strain PCC 7120. Mol Microbiol 77:562–574PubMedCrossRefGoogle Scholar
  74. Higa KC, Rajagopalan R, Risser DD, Rivers OS, Tom SK, Videau P, Callahan SM (2012) The RGSGR amino acid motif of the intercellular signalling protein, HetN, is required for patterning of heterocysts in Anabaena sp. strain PCC 7120. Mol Microbiol 83:682–693PubMedCrossRefGoogle Scholar
  75. Houchins JP (1984) The physiology and biochemistry of hydrogen metabolism in cyanobacteria. Biochim Biophys Acta 768:227–255CrossRefGoogle Scholar
  76. Houchins JP, Burris RH (1981a) Comparative characterization of two distinct hydrogenases from Anabaena sp. strain 7120. J Bacteriol 146:215–221PubMedPubMedCentralGoogle Scholar
  77. Houchins JP, Burris RH (1981b) Occurrence and localization of two distinct hydrogenases in the heterocystous cyanobacterium Anabaena sp. strain 7120. J Bacteriol 146:209–214PubMedPubMedCentralGoogle Scholar
  78. Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96:2965–2982PubMedCrossRefGoogle Scholar
  79. Howarth DC, Codd GA (1985) The uptake and production of molecular hydrogen by unicellular cyanobacteria. J Gen Microbiol 131:1561–1569Google Scholar
  80. Howitt CA, Vermaas WFJ (1999) Subunits of the NAD(P)- reducing nickel-containing hydrogenase do not act as part of the type-1 NAD(P)H-dehydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. In: Peschek GA, Löffelhardt W, Schmetterer G (eds) The phototrophic prokaryotes. Kluwer, New York, pp 595–601CrossRefGoogle Scholar
  81. Huang HH, Camsund D, Lindblad P, Heidorn T (2010) Design and characterization of molecular tools for a synthetic biology approach towards developing cyanobacterial biotechnology. Nucleic Acids Res 38:2577–2593PubMedPubMedCentralCrossRefGoogle Scholar
  82. Hydrogen Fuel Cells Program (2009) Annual report. Department of Energy, USAGoogle Scholar
  83. Jeffries TW, Timourian H, Ward RL (1978) Hydrogen production by Anabaena cylindrica: effects of varying ammonium and ferric ions, pH, and light. Appl Environ Microbiol 35:704–710PubMedPubMedCentralGoogle Scholar
  84. Jones KM, Haselkorn R (2002) Newly identified cytochrome c oxidase operon in the nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 specifically induced in heterocysts. J Bacteriol 184:2491–2499PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kaneko T, Tabata S (1997) Complete genome structure of the unicellular cyanobacterium Synechocystis sp. PCC6803. Plant Cell Physiol 38:1171–1176PubMedCrossRefGoogle Scholar
  86. Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M, Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213PubMedCrossRefGoogle Scholar
  87. Kentemich T, Bahnweg M, Mayer F, Bothe H (1989) Localization of the reversible hydrogenase in cyanobacteria. Z Naturforsch 44:384–391Google Scholar
  88. Khetkorn W, Khanna N, Incharoensakdi A, Lindblad P (2013) Metabolic and genetic engineering for enhanced hydrogen production. Biofuels 4:535–561CrossRefGoogle Scholar
  89. Khudyakov I, Wolk CP (1997) hetC, a gene coding for a protein similar to bacterial ABC protein exporters, is involved in early regulation of heterocyst differentiation in Anabaena sp. strain PCC 7120. J Bacteriol 179:6971–6978PubMedPubMedCentralGoogle Scholar
  90. Kim CH, Newton WE, Dean DR (1995) Role of the MoFe protein alpha-subunit histidine-195 residue in FeMo-cofactor binding and nitrogenase catalysis. Biochemistry 34:2798–2808PubMedCrossRefGoogle Scholar
  91. Kumar K, Mella-Herrera R, Golden JW (2010) Cyanobacterial heterocysts. Cold Spring Harb Perspect Biol 2:a000315PubMedPubMedCentralCrossRefGoogle Scholar
  92. Kumaraswamy KG, Guerra T, Qian X, Zhang S, Bryant D, Dismukes GC (2013) Reprogramming the glycolytic pathway for increased hydrogen production in cyanobacteria: metabolic engineering of NAD+-dependent GAPDH. Energy Environ Sci 6:3722–3731CrossRefGoogle Scholar
  93. Lambert GR, Smith GD (1977) Hydrogen formation by marine blue–green algae. FEBS Lett 83:159–162PubMedCrossRefGoogle Scholar
  94. Lambert GR, Daday A, Smith GD (1979) Duration of hydrogen formation by Anabaena cylindrica B629 in atmospheres of argon, air, and nitrogen. Appl Environ Microbiol 38:530–536PubMedPubMedCentralGoogle Scholar
  95. Leroux F, Dementin S, Burlat B, Cournac L, Volbeda A, Champ S, Martin L, Guigliarelli B, Bertrand P, Fontecilla-Camps P, Rousset M, Léger C (2008) Experimental approaches to kinetics of gas diffusion in hydrogenase. Proc Natl Acad Sci U S A 105:11188–11193PubMedPubMedCentralCrossRefGoogle Scholar
  96. Liang J, Scappino L, Haselkorn R (1992) The patA gene product, which contains a region similar to CheY of Escherichia coli, controls heterocyst pattern formation in the cyanobacterium Anabaena 7120. Proc Natl Acad Sci U S A 89:5655–5659PubMedPubMedCentralCrossRefGoogle Scholar
  97. Lindberg P (2003) Cyanobacterial hydrogen metabolism – uptake hydrogenase and hydrogen production by nitrogenase in filamentous cyanobacteria. PhD-thesis, Uppsala University, SwedenGoogle Scholar
  98. Lindberg P, Hansel A, Lindblad P (2000) hupS and hupL constitute a transcription unit in the cyanobacterium Nostoc sp. PCC 73102. Arch Microbiol 174:129–133PubMedCrossRefGoogle Scholar
  99. Lindberg P, Schütz K, Happe T, Lindblad P (2002) A hydrogen-producing, hydrogenase-free mutant strain of Nostoc punctiforme ATCC 29133. Int J Hydrogen Energy 27:1291–1296CrossRefGoogle Scholar
  100. Lopes FA, Troshina O, Lindblad P (2002) A brief look at three decades of research on cyanobacterial hydrogen evolution. Int J Hydrogen Energy 27:1209–1215CrossRefGoogle Scholar
  101. Lukey MJ, Parkin A, Roessler MM, Murphy BJ, Harmer J, Palmer T, Sargent F, Armstrong FA (2010) How Escherichia coli is equipped to oxidize hydrogen under different redox conditions. J Biol Chem 285:3928–3938PubMedPubMedCentralCrossRefGoogle Scholar
  102. Maldener I, Fiedler G, Ernst A, Fernández-Piñas F, Wolk CP (1994) Characterization of devA, a gene required for the maturation of proheterocysts in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 176:7543–7549PubMedPubMedCentralGoogle Scholar
  103. Martinho R (2009) Immunolocalization of the uptake hydrogenase in cyanobacteria: uptake hydrogenase in the marine Lyngbya majuscula CCAP 1446/4 and Nostoc spp. VDM, Verlag, Saarbrücken, p 60Google Scholar
  104. Masepohl B, Schölisch K, Görlitz K, Kutzki C, Bohme 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 253:770–776PubMedCrossRefGoogle Scholar
  105. Masukawa H, Nakamura K, Mochimaru M, Sakurai H (2001) Photobiological hydrogen production and nitrogenase activity in some heterocystous cyanobacteria. In: Miyake J, Matsunaga T, San Pietro A (eds) Biohydrogen II. Elsevier, Oxford, pp 63–66CrossRefGoogle Scholar
  106. Masukawa H, Inoue K, Sakurai H, Wolk CP, Hausinger RP (2010) Site-directed mutagenesis of the Anabaena sp. strain PCC 7120 nitrogenase active site to increase photobiological hydrogen production. Appl Environ Microbiol 76:6741–6750PubMedPubMedCentralCrossRefGoogle Scholar
  107. Mata TM, Martins A, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sustain Energy Rev 14:217–232CrossRefGoogle Scholar
  108. McNeely K, Xu Y, Bennette N, Bryant D, Dismukes GC (2010) Redirecting reductant flux into hydrogen production via metabolic engineering of fermentative carbon metabolism in a cyanobacterium. Appl Environ Microbiol 76:5032–5038PubMedPubMedCentralCrossRefGoogle Scholar
  109. Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106PubMedCrossRefGoogle Scholar
  110. Meeks JC, Campbell EL, Summers ML, Wong FC (2002) Cellular differentiation in the cyanobacterium Nostoc punctiforme. Arch Microbiol 178:395–403PubMedCrossRefGoogle Scholar
  111. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–136PubMedPubMedCentralCrossRefGoogle Scholar
  112. Merino-Puerto V, Mariscal V, Schwarz H, Maldener I, Mullineaux CW, Herrero A, Flores E (2011) FraH is required for reorganization of intracellular membranes during heterocyst differentiation in Anabaena sp. strain PCC 7120. J Bacteriol 193:6815–6823PubMedPubMedCentralCrossRefGoogle Scholar
  113. Min HT, Sherman LA (2010) Hydrogen production by the unicellular, diazotrophic cyanobacterium Cyanothece sp. strain ATCC 51142 under conditions of continuous light. Appl Environ Microbiol 76:4293–4301PubMedPubMedCentralCrossRefGoogle Scholar
  114. Mulligan ME, Haselkorn R (1989) Nitrogen fixation (nif) genes of the cyanobacterium Anabaena species strain PCC 7120. The nifB-fdxN-nifS-nifU operon. J Biol Chem 264:19200–19207PubMedGoogle Scholar
  115. Muro-Pastor AM, Valladares A, Flores E, Herrero A (1999) The hetC gene is a direct target of the NtcA transcriptional regulator in cyanobacterial heterocyst development. J Bacteriol 181:6664–6669PubMedPubMedCentralGoogle Scholar
  116. Muro-Pastor AM, Valladares A, Flores E, Herrero A (2002) Mutual dependence of the expression of the cell differentiation regulatory protein HetR and the global nitrogen regulator NtcA during heterocyst development. Mol Microbiol 44:1377–1385PubMedCrossRefGoogle Scholar
  117. Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282:25475–25486PubMedCrossRefGoogle Scholar
  118. Neunuebel MR, Golden JW (2008) The Anabaena sp. strain PCC 7120 gene all2874 encodes a diguanylate cyclase and is required for normal heterocyst development under high-light growth conditions. J Bacteriol 190:6829–6836PubMedPubMedCentralCrossRefGoogle Scholar
  119. Nguyen AV, Thomas-Hall SR, Malnoë A, Timmins M, Mussgnug JH, Rupprecht J, Kruse O, Hankamer B, Schenk PM (2008) Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 7:1965–1979PubMedPubMedCentralCrossRefGoogle Scholar
  120. Ohki K, Taniuchi Y (2009) Detection of nitrogenase in individual cells of a natural population of Trichodesmium using immunocytochemical methods for fluorescent cells. J Oceanogr 65:427–432CrossRefGoogle Scholar
  121. Oliveira P, Lindblad P (2005) LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 251:59–66PubMedCrossRefGoogle Scholar
  122. Oliveira P, Lindblad P (2008) An AbrB-Like protein regulates the expression of the bidirectional hydrogenase in Synechocystis sp. strain PCC 6803. J Bacteriol 190:1011–1019PubMedPubMedCentralCrossRefGoogle Scholar
  123. Oliveira P, Leitão E, Tamagnini P, Moradas-Ferreira P, Oxelfelt F (2004) Characterization and transcriptional analysis of hupSLW in Gloeothece sp. ATCC 27152: an uptake hydrogenase from a unicellular cyanobacterium. Microbiology 150:3647–3655PubMedCrossRefGoogle Scholar
  124. Orozco CC, Risser DD, Callahan SM (2006) Epistasis analysis of four genes from Anabaena sp. strain PCC 7120 suggests a connection between PatA and PatS in heterocyst pattern formation. J Bacteriol 188:1808–1816PubMedPubMedCentralCrossRefGoogle Scholar
  125. Ow SY, Cardona T, Taton A, Magnuson A, Lindblad P, Stensjö K, Wright PC (2008) Quantitative shotgun proteomics of enriched heterocysts from Nostoc sp. PCC 7120 using 8-plex isobaric peptide tags. J Proteome Res 7:1615–1628PubMedCrossRefGoogle Scholar
  126. Oxelfelt F, Tamagnini P, Salema R, Lindblad P (1995) Hydrogen uptake in Nostoc strain PCC 73102: effects of nickel, hydrogen, carbon and nitrogen. Plant Physiol Biochem 33:617–623Google Scholar
  127. Pandelia ME, Nitschke W, Infossi P, Giudici-Orticoni MT, Bill E, Lubitz W (2011) Characterization of a unique [FeS] cluster in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus. Proc Natl Acad Sci U S A 108:6097–6102PubMedPubMedCentralCrossRefGoogle Scholar
  128. Papen H, Kentemich T, Schmülling T, Bothe H (1986) Hydrogenase activities in cyanobacteria. Biochimie 68:121–132PubMedCrossRefGoogle Scholar
  129. Parmar A, Singh NK, Pandey A, Gnansounou E, Madamwar D (2011) Cyanobacteria and microalgae: a positive prospect for biofuels. Bioresour Technol 102:10163–10172PubMedCrossRefGoogle Scholar
  130. Pastor AM, Hess WR (2012) Heterocyst differentiation: from single mutants to global approaches. Trends Microbiol 20:548–557CrossRefGoogle Scholar
  131. Penfold DW, Sargent F, Macaskie LE (2006) Inactivation of the Escherichia coli K-12 twin-arginine translocation system promotes increased hydrogen production. FEMS Microbiol Lett 262:135–137PubMedCrossRefGoogle Scholar
  132. Pinto F, Van Elburg K, Pacheco CC, Lopo M, Noirel J, Montagud A, Urchueguía JF et al (2012) Construction of a chassis for hydrogen production: physiological and molecular characterization of a Synechocystis sp. PCC 6803 mutant lacking a functional bidirectional hydrogenase. Microbiology 158:448–464PubMedCrossRefGoogle Scholar
  133. Pisciotta JM, Zou Y, Baskakov IV (2010) Light-dependent electrogenic activity of cyanobacteria. PLoS One 5:e10821PubMedPubMedCentralCrossRefGoogle Scholar
  134. Postgate JR (1998) Nitrogen fixation. Cambridge University Press, Cambridge, 112 ppGoogle Scholar
  135. Rakhely G, Kovacs A, Maroti G, Fodor BD, Csanadi G, Latinovics D, Kovacs KL (2004) Cyanobacterial-type, pentameric, NAD-reducing NiFe hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 70:722–728PubMedPubMedCentralCrossRefGoogle Scholar
  136. Ramasubramanian TS, Wei TF, Golden JW (1994) Two Anabaena sp. strain PCC 7120 DNA-binding factors interact with vegetative cell- and heterocyst-specific genes. J Bacteriol 176:1214–1223PubMedPubMedCentralGoogle Scholar
  137. Razquin P, Schmitz S, Fillat MF, Peleato ML, Böhme H (1994) Transcriptional and translational analysis of ferredoxin and flavodoxin under iron and nitrogen stress in Anabaena sp. strain PCC 7120. J Bacteriol 176:7409–7411PubMedPubMedCentralGoogle Scholar
  138. Reddy KJ, Haskell JB, Sherman DM, Sherman LA (1993) Unicellular, aerobic nitrogen-fixing cyanobacteria of the genus Cyanothece. J Bacteriol 175:1284–1292PubMedPubMedCentralGoogle Scholar
  139. Risser DD, Callahan SM (2008) HetF and PatA control levels of HetR in Anabaena sp. strain PCC 7120. J Bacteriol 190:7645–7654PubMedPubMedCentralCrossRefGoogle Scholar
  140. Rögner M, Nixon P, Diner B (1990) Purification and characterization of photosystem I and photosystem II core complexes from wild- type and phycocyanin-deficient strains of the cyanobacterium Synechocystis PCC 6803. J Biol Chem 265:6189–6196PubMedGoogle Scholar
  141. Roseboom W, De Lacey AL, Fernandez VM, Hatchikian EC, Albracht SP (2006) The active site of the [FeFe]-hydrogenase from Desulfovibrio desulfuricans. II. Redox properties, light sensitivity and CO-ligand exchange as observed by infrared spectroscopy. J Biol Inorg Chem 11:102–118PubMedCrossRefGoogle Scholar
  142. Sakr S, Dutheil J, Saenkham R, Bottin H, Leplat C, Ortega-Ramos M, Aude JC, Chapuis V, Guedeney G, Decottignies P, Lemaire S, Cassier-Chauvat C, Chauvat F (2013) The activity of the Synechocystis PCC6803 AbrB2 regulator of hdyrogen peouction can be post-translatonally controlled through glutathionylation. Int J Hydrogen Energy 38:13547–13555CrossRefGoogle Scholar
  143. Sawers R, Blokesch M, Böck A (2004) Anaerobic formate and hydrogen metabolism. EcoSal Plus. doi: 10.1128/ecosalplus.3.5.4
  144. Schmitz O, Bothe H (1996) The diaphorase subunit HoxU of the bidirectional hydrogenase as electron transferring protein in cyanobacterial respiration? Naturwissenschaften 83:525–527PubMedCrossRefGoogle Scholar
  145. Schmitz O, Boison G, Hilscher R, Hundeshagen B, Zimmer W, Lottspeich F, Bothe H (1995) Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria. Eur J Biochem 233:266–276PubMedCrossRefGoogle Scholar
  146. Schmitz O, Boison G, Salzmann H, Bothe H, Schütz K, Wang S, Happe T (2002) HoxE—a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim Biophys Acta 1554:66–74PubMedCrossRefGoogle Scholar
  147. Schneider K, Schlegel HG (1976) Purification and properties of the soluble hydrogenase from Alcaligenes eutrophus H16. Biochim Biophys Acta 452:66–80PubMedCrossRefGoogle Scholar
  148. Schrautemeier B, Böhme H (1985) A distinct ferredoxin for nitrogen fixation isolated from heterocysts of the cyanobacterium Anabaena variabilis. FEBS Lett 184:304–308CrossRefGoogle Scholar
  149. Serebriakova LT, Zorin NA, Lindblad P (1994) Reversible hydrogenase in Anabaena variabilis ATCC 29413: presence and localization in non-N2-fixing cells. Arch Microbiol 161:140–144Google Scholar
  150. Shen G, Boussiba S, Vermaas WF (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1853–1863PubMedPubMedCentralCrossRefGoogle Scholar
  151. Sheremetieva ME, Troshina OY, Serebryakova LT, Lindblad P (2002) Identification of hox genes and analysis of their transcription in the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 growing under nitrate-limiting conditions. FEMS Microbiol Lett 214:229–233PubMedCrossRefGoogle Scholar
  152. Shi Y, Zhao W, Zhang W, Ye Z, Zhao J (2006) Regulation of intracellular free calcium concentration during heterocyst differentiation by HetR and NtcA in Anabaena sp. PCC 7120. Proc Natl Acad Sci U S A 103:11334–11339PubMedPubMedCentralCrossRefGoogle Scholar
  153. Sjöholm J, Oliveira P, Lindblad P (2007) Transcription and regulation of the bidirectional hydrogenase in the cyanobacterium Nostoc sp. strain PCC 7120. Appl Environ Microbiol 73:5435–5446PubMedPubMedCentralCrossRefGoogle Scholar
  154. Skizim NJ, Ananyev GM, Krishnan A, Dismukes GC (2012) Metabolic pathways for photobiological hydrogen production by nitrogenase- and hydrogenase-containing unicellular cyanobacteria Cyanothece. J Biol Chem 287:2777–2786PubMedPubMedCentralCrossRefGoogle Scholar
  155. Spatzal T, Aksoyoglu M, Zhang L, Andrade SL, Schleicher E, Weber S, Rees DC, Einsle O (2011) Evidence for interstitial carbon in nitrogenase FeMo cofactor. Science 334:940PubMedPubMedCentralCrossRefGoogle Scholar
  156. Staff reporter, Japanese group to market hydrogen fuel made from sewage (2012) ( ENVIRONMENT
  157. Stephenson M, Stickland LH (1931) Hydrogenase: a bacterial enzyme activating molecular hydrogen: the properties of the enzyme. Biochem J 25:205–214PubMedPubMedCentralCrossRefGoogle Scholar
  158. Tamagnini P, Axelsson R, Lindberg P, Wünschiers R, Lindblad P, Oxelfelt F (2002) Hydrogenases and hydrogen metabolism of cyanobacteria hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66:1–20PubMedPubMedCentralCrossRefGoogle Scholar
  159. Tamagnini P, Leitão E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720PubMedCrossRefGoogle Scholar
  160. Tanksale A, Beltramini JN, Lu GM (2010) A review of catalytic hydrogen production processes from biomass. Renew Sustain Energy Rev 14:166–182CrossRefGoogle Scholar
  161. The European Strategic Energy Technology Plan – SET-Plan: towards a low-carbon future (2008) Annual report. Publications Office of the European Union, LuxembourgGoogle Scholar
  162. Thiel T (1993) Characterization of genes for an alternative nitrogenase in the cyanobacterium Anabaena variabilis. J Bacteriol 175:6276–6286PubMedPubMedCentralGoogle Scholar
  163. Thiel T, Lyons EM, Erker JC (1997) Characterization of genes for a second Mo-dependent nitrogenase in the cyanobacterium Anabaena variabilis. J Bacteriol 179:5222–5225PubMedPubMedCentralGoogle Scholar
  164. Toepel J, McDermott JE, Summerfield TC, Sherman LA (2009) Transcriptional analysis of the unicellular, diazotrophic cyanobacterium Cyanothece sp. ATCC 51142 grown under short day/night cycles. J Phycol 45:610–620CrossRefGoogle Scholar
  165. Torrecilla I, Leganés F, Bonilla I, Fernández-Piñas F (2004) A calcium signal is involved in heterocyst differentiation in the cyanobacterium Anabaena sp. PCC7120. Microbiology 150:3731–3739PubMedCrossRefGoogle Scholar
  166. Tracking clean energy progress (2013) Annual report. International Energy Agency, FranceGoogle Scholar
  167. Troshina O, Serebryakova L, Sheremetieva M, Lindblad P (2002) Production of H2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. Int J Hydrogen Energy 27:1283–1289CrossRefGoogle Scholar
  168. Vignais PM, Billoud B (2007) Occurrence, classification and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272PubMedCrossRefGoogle Scholar
  169. Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188PubMedGoogle Scholar
  170. Vignais PM, Cournac L, Hatchikian EC, Elsen S, Serebryakova L, Zorin N, Dimon B (2002) Continuous monitoring of the activation and activity of NiFe-hydrogenases by membrane-inlet mass spectrometry. Int J Hydrogen Energy 27:1441–1448CrossRefGoogle Scholar
  171. Watt GD, Bulen WA, Burns A, Hadfield KL (1975) Stoichiometry, ATP/2e values, and energy requirements for reactions catalyzed by nitrogenase from Azotobacter vinelandii. Biochemistry 14:4266–4272PubMedCrossRefGoogle Scholar
  172. Weissman JC, Benemann JR (1977) Hydrogen production by nitrogen-starved cultures of Anabaena cylindrica. Appl Environ Microbiol 33:123–131PubMedPubMedCentralGoogle Scholar
  173. Weyman PD, Pratte B, Thiel T (2008) Transcription of hupSL in Anabaena variabilis ATTC 29143 is regulated by NtcA and not by hydrogen. Appl Environ Microbiol 74:2103–2110PubMedPubMedCentralCrossRefGoogle Scholar
  174. Wong FC, Meeks JC (2001) The hetF gene product is essential to heterocyst differentiation and affects HetR function in the cyanobacterium Nostoc punctiforme. J Bacteriol 183:2654–2661PubMedPubMedCentralCrossRefGoogle Scholar
  175. Woodward J, Orr M, Cordray K, Greenbaum E (2000) Enzymatic production of biohydrogen. Nature 405:1014–1015PubMedCrossRefGoogle Scholar
  176. Wu X, Liu D, Lee MH, Golden JW (2004) patS minigenes inhibit heterocyst development of Anabaena sp. train PCC 7120. J Bacteriol 186:6422–6429PubMedPubMedCentralCrossRefGoogle Scholar
  177. Wulff P, Day CC, Sargent F, Armstrong FA (2014) How oxygen reacts with oxygen-tolerant respiratory [NiFe]-hydrogenases. Proc Natl Acad Sci U S A 111:6606–6611PubMedPubMedCentralCrossRefGoogle Scholar
  178. Yeager CM, Milliken CE, Bagwell CE, Staples L, Berseth PA, Sessions HT (2011) Evaluation of experimental conditions that influence hydrogen production among heterocystous cyanobacteria. Int J Hydrogen Energy 36:7487–7499CrossRefGoogle Scholar
  179. Yoon HS, Golden JW (1975) Heterocyst pattern-formation controlled by a diffusible peptide. Science 282:935–938CrossRefGoogle Scholar
  180. Yoshino F, Ikeda H, Masukawa H, Sakurai H (2007) High photobiological hydrogen production activity of a Nostoc sp. PCC 7422 uptake hydrogenase-deficient mutant with high nitrogenase activity. Mar Biotechnol 9:101–112PubMedCrossRefGoogle Scholar
  181. Yu Y, You L, Liu D, Hollinshead W, Tang YJ, Zhang F (2013) Development of Synechocystis sp. PCC 6803 as a phototrophic cell factory. Mar Drugs 11:2894–2916PubMedPubMedCentralCrossRefGoogle Scholar
  182. Zehr P, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity in the environment. Environ Microbiol 5:539–554PubMedCrossRefGoogle Scholar
  183. Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322:1110–1112PubMedCrossRefGoogle Scholar
  184. Zhang Z, Pendse N, Phillips KN, Cotner JB, Khodursky A (2008) Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics 14:1–14CrossRefGoogle Scholar
  185. Zhao Y, Shi Y, Zhao W, Huang X, Wang D, Brown N, Brand J, Zhao J (2005) CcbP, a calcium-binding protein from Anabaena sp. PCC 7120, provides evidence that calcium ions regulate heterocyst differentiation. Proc Natl Acad Sci U S A 102:5744–5748PubMedPubMedCentralCrossRefGoogle Scholar
  186. Zhou R, Wolk CP (2003) A two-component system mediates developmental regulation of biosynthesis of a heterocyst polysaccharide. J Biol Chem 278:19939–19946PubMedCrossRefGoogle Scholar
  187. Zhou R, Wei X, Jiang N, Li H, Dong Y, Hsi KL, Zhao J (1998) Evidence that HetR protein is an unusual serine-type protease. Proc Natl Acad Sci U S A 95:4959–4963PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Namita Khanna
    • 1
  • Patrícia Raleiras
    • 1
  • Peter Lindblad
    • 1
    Email author
  1. 1.Microbial Chemistry, Department of Chemistry – Ångström LaboratoryUppsala UniversityUppsalaSweden

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