Cyanobacteria are photoautotrophic prokaryotes with a remarkable metabolic flexibility. Many species of cyanobacteria produce hydrogen, and the efficiency of this process can be improved by genetic engineering. Isolated photosynthetic complexes of cyanobacteria that are capable of light absorption and charge separation can be utilized in hydrogen-producing devices that are driven by solar energy. As photosynthetic microorganisms, cyanobacteria present a unique opportunity for creating low cost systems for hydrogen production in vivo and in vitro. This review is focused on recent advances in cyanobacterial hydrogen research.
References
[1]
J. W. Schopf, “The Paleobiological Record of Photosynthesis,” Photosynthesis Research, Vol. 107, No. 1, 2011, pp. 87-101. http://dx.doi.org/10.1007/s11120-010-9577-1
[2]
R. Saha, A. T. Verseput, B. M. Berla, T. J. Mueller, H. B. Pakrasi and C. D. Maranas, “Reconstruction and Comparison of the Metabolic Potential of Cyanobacteria Cyanothece sp. ATCC 51142 and Synechocystis sp. PCC 6803,” PLoS ONE, Vol. 7, No. 10, 2012, Article ID: e48285. http://dx.doi.org/10.1371/journal.pone.0048285
[3]
P. P. Edwards, V. L. Kuznetsov and W. I. F. David, “Hydrogen Energy,” Philosophical Transactions of the Royal Society, Vol. 365, No. 1853, 2007, pp. 1043-1056. http://dx.doi.org/10.1098/rsta.2006.1965
[4]
D. Dutta, D. De, S. Chaudhuri and S. K. Bhattacharya, “Hydrogen Production by Cyanobacteria,” Microbial Cell Factories, Vol. 4, 2005, p. 36. http://dx.doi.org/10.1186/1475-2859-4-36
[5]
J. Mathews and G. Wang, “Metabolic Pathway Engineering for Enhanced Hydrogen Production,” International Journal of Hydrogen Energy, Vol. 34, No. 17, 2009, pp. 7404-7416. http://dx.doi.org/10.1016/j.ijhydene.2009.05.078
[6]
J. Appel and R. Schulz, “Hydrogen Metabolism in Organisms with Oxygenic Photosynthesis: Hydrogenases as Important Regulatory Devices for a Proper Redox Poising?” Journal of Photochemistry and Photobiology, Vol. 47, No. 1, 1998, pp.1-11. http://dx.doi.org/10.1016/S1011-1344(98)00179-1
[7]
M. Ludwig, R. Schulz-Friedrich and J. Appel, “Occurrence of Hydrogenases in Cyanobacteria and Anoxygenic Photosynthetic Bacteria: Implications for the Phylogenetic Origin of Cyanobacterial and Algal Hydrogenases,” Journal of Molecular Evolution, Vol. 63, No. 6, 2006, pp. 758-768. http://dx.doi.org/10.1007/s00239-006-0001-6
[8]
S. V. Shestakov and L. E. Mikheeva, “Genetic Control of Hydrogen Metabolism in Cyanobacteria”, Russian Journal of Genetics, Vol. 42, No. 11, 2006, pp. 1272-1284. http://dx.doi.org/10.1134/S1022795406110093
[9]
R. Wünschiers, M. Batur and P. Lindblad, “Presence and Expression of Hydrogenase Specific C-Terminal Endopeptidases in Cyanobacteria,” BMC Microbiology, Vol. 3, 2003, p. 8. http://dx.doi.org/10.1186/1471-2180-3-8
[10]
F. Germer, I. Zebger, M. Saggu, F. Lendzian, R. Schulz and J. Appel, “Overexpression, Isolation, and Spectroscopic Characterization of the Bidirectional [NiFe] Hydrogenase from Synechocystis sp. PCC 6803,” Journal of Biological Chemistry, Vol. 284, No. 52, 2009, pp. 36462-36472. http://dx.doi.org/10.1074/jbc.M109.028795
[11]
L. Cournac, G. Guedeney, G. Peltier and P. M. Vignais, “Sustained Photoevolution of Molecular Hydrogen in a Mutant of Synechocystis sp. strain PCC 6803 Deficient in the Type I NADPH-Dehydrogenase Complex,” Journal of Bacteriology, Vol. 186, No. 6, 2004, pp. 1737-1746. http://dx.doi.org/10.1128/JB.186.6.1737-1746.2003
[12]
O. Schmitz, G. Boison, R. Hilscher, B. Hundeshagen, W. Zimmer, F. Lottspeich, and H. Bothe, “Molecular Biological Analysis of a Bidirectional Hydrogenase from Cyanobacteria,” European Journal of Biochemistry, Vol. 233, No. 1, 1995, pp. 266-276. http://dx.doi.org/10.1111/j.1432-1033.1995.266_1.x
[13]
J. Appel, S. Phunpruch, K. Steinmüller and R. Schulz, “The Bidirectional Hydrogenase of Synechocystis sp. PCC 6803 Works as an Electron Valve During Photosynthesis,” Archives of Microbiology, Vol. 173, No. 5-6, 2000, pp. 333-338. http://dx.doi.org/10.1007/s002030000139
[14]
P. Tamagnini, O. Troshina, F. Oxelfelt, R. Salema and P. Lindblad, “Hydrogenases in Nostoc sp. Strain PCC 73102, a Strain Lacking a Bidirectional Enzyme,” Applied Environmental Microbiology, Vol. 63, No. 5, 1997, pp. 1801-1807.
[15]
T. Kentemich, M. Bahnweg, F. Mayer and H. Bothe, “Localization of the Reversible Hydrogenase in Cyanobacteria,” Zeitschrift für Naturforschung C, A Journal of Biological Sciences, Vol. 44c, 1989, pp. 384-391.
[16]
L. Serebriakova, N. A. Zorin and P. Lindblad, “Reversible Hydrogenase in Anabaena variabilis ATCC 29413: Presence and Localization in Non-N2-Fixing Cells,” Archives of Microbiology, Vol. 161, No. 2, 1994, pp. 140-144. http://dx.doi.org/10.1007/BF00276474
[17]
K. McNeely, Y. Xu, G. Ananyev, N. Bennette, D. A. Bryant and G. C. Dismukes, “Synechococcus sp. Strain PCC 7002 nifJ Mutant Lacking Pyruvate: Ferredoxin Oxidoreductase,” Applied Environmental Microbiology, Vol. 77, No. 7, 2011, pp. 2435-2444. http://dx.doi.org/10.1128/AEM.02792-10
[18]
P. Tamagnini, J.-L. Costa, L. Almeida, M.-J. Oliveira, R. Salema and P. Lindblad, “Diversity of Cyanobacterial Hydrogenases, a Molecular Approach,” Current Microbiology, Vol. 40, No. 6, 2000, pp. 356-361. http://dx.doi.org/10.1007/s002840010070
[19]
P. M. Vignais, B. Billoud and J. Meyer, “Classification and Phylogeny of Hydrogenases,” FEMS Microbiology Reviews, Vol. 25, No. 4, 2001, pp. 455-501. http://dx.doi.org/10.1016/S0168-6445(01)00063-8
[20]
P. Tamagnini, R. Axelsson, P. Lindberg, F. Oxelfelt, R. Wunschiers and P. Lindblad, “Hydrogenases and Hydrogen Metabolism of Cyanobacteria,” Microbiology and Molecular Biology Reviews, Vol. 66, No. 1, 2002, pp. 1-20. http://dx.doi.org/10.1128/MMBR.66.1.1-20.2002
[21]
L. E. Mikheeva, O. Schmitz, S. V. Shestakov and H. Bothe, “Mutants of the Cyanobacterium Anabaena variabilis Altered in Hydrogenase Activities,” Zeitschrift für Naturforschung C, A Journal of Biological Sciences, Vol. 50c, 1995, pp. 505-510.
[22]
T. Happe, K. Schutz and H. Bohme, “Transcriptional and Mutational Analysis of the Uptake Hydrogenase of the Filamentous Cyanobacterium Anabaena variabilis ATCC 29413,” Journal of Bacteriology, Vol. 182, No. 6, 2000, pp. 1624-1631. http://dx.doi.org/10.1128/JB.182.6.1624-1631.2000
[23]
H. Masukawa, M. Mochimaru and H. Sakurai, “Disruption of the Uptake Hydrogenase Gene, but not of the Bidirectional Hydrogenase Gene, Leads to Enhanced Photobiological Hydrogen Production by the NitrogenFixing Cyanobacterium Anabaena sp. PCC 7120,” Applied Microbiology and Biotechnology, Vol. 58, No. 5, 2002, pp. 618-624. http://dx.doi.org/10.1007/s00253-002-0934-7
[24]
W. Khetkorn, P. Lindblad and A. Incharoensakdi, “Inactivation of Uptake Hydrogenase Leads to Enhanced and Sustained Hydrogen Production with High Nitrogenase Activity under High Light Exposure in the Cyanobacte rium Anabaena siamensis TISTR 8012,” Journal of Biological Engineering, Vol. 6, 2012, p. 19. http://dx.doi.org/10.1186/1754-1611-6-19
[25]
F. Yoshino, H. Ikeda, H. Masukawa and H. Sakurai, “High Photobiological Hydrogen Production Activity of a Nostoc sp. PCC 7422 Uptake Hydrogenase-Deficient Mutant with High Nitrogenase Activity,” Marine Biotechnology, Vol. 9, No. 1, 2007, pp. 101-112. http://dx.doi.org/10.1007/s10126-006-6035-3
[26]
L. A. Sherman, H. Min, J. Toepel and H. B. Pakrasi, “Better Living Through Cyanothece—Unicellular Diazotrophic Cyanobacteria with Highly Versatile Metabolic Systems,” Advances in Experimental Medicine and Biology, Vol. 675, 2010, pp. 275-90. http://dx.doi.org/10.1007/978-1-4419-1528-3_16
[27]
H. Masukawa, K. Inoue and H. Sakurai, “Effects of Disruption of Homocitrate Synthase Genes on Nostoc sp. Strain PCC 7120 Photobiological Hydrogen Production and Nitrogenase,” Applied and Environmental Microbiology, Vol. 73, No. 23, 2007, pp. 7562-7570. http://dx.doi.org/10.1128/AEM.01160-07
[28]
H. Masukawa, K. Inoue, H. Sakurai, C. P. Wolk and R. P. Hausinger, “Site-Directed Mutagenesis of the Anabaena sp. Strain PCC 7120 Nitrogenase Active Site to Increase Photobiological Hydrogen Production,” Applied and Environmental Microbiology, Vol. 76, No. 20, 2010, pp. 6741-6750. http://dx.doi.org/10.1128/AEM.01056-10
[29]
C. P. Wolk, A. Ernst and J. Elhai, “Heterocyst Metabolism and Development,” In: D. A. Bryant, Ed., The Molecular Biology of Cyanobacteria, Kluwer Academic Publishers, Netherlands, 1994, pp. 769-823. http://dx.doi.org/10.1007/978-94-011-0227-8_27
[30]
D. A. Sveshnikov, N. V. Sveshnikova, K. K. Rao and D. O. Hall, “Hydrogen Metabolism of Mutant Forms of Anabaena variabilis in Continuous Cultures and under Nutritional Stress,” FEMS Microbiology Letters, Vol. 147, No. 2, 1997, pp. 297-301.
[31]
F. Yoshino, H. Ikeda, H. Masukawa and H. Sakurai, “High Photobiological Hydrogen Production Activity of Nostoc sp. PCC 7422 Uptake Hydrogenase-Deficient Mutant with High Nitrogenase Activity,” Marine Biotechnology, Vol. 9, No. 1, 2007, pp.101-112. http://dx.doi.org/10.1007/s10126-006-6035-3
[32]
H. Christman, E. Campbell, D. Risser, B. Phinney, W.-L. Chiu and J. C. Meeks, “Systems Level Approaches To Understanding And Manipulating Heterocyst Differentiation in Nostoc punctiforme: Sites of Hydrogenase and Nitrogenase Synthesis and Activity,” Proceedings of the 2012 Department of Energy (DOE) Genomic Science Program Awardee Meeting, Bethesda, 26-29 February 2012, p. 72.
[33]
J. Yu and H. Takahashi, “Biophotolysis-Based Hydrogen Production by Cyanobacteria and Green Microalgae,” In: A. Méndez-Vilas, Ed., Communicating Current Research and Educational Topics and Trends in Applied Microbiology, Formatex, 2007, pp. 79-89.
[34]
J. P. H. Reade, L. I. Dougherty, L. J. Rogers and J. R. Gallon, “Synthesis and Proteolytic Degradation of Nitrogenase in Cultures of the Unicellular Cyanobacterium Gloeothece Strain ATCC 27152,” Microbiology, Vol. 145, No. 7, 1999, pp. 1749-1758. http://dx.doi.org/10.1099/13500872-145-7-1749
[35]
L. A. Sherman, P. Meunier, M. S. Colón-López, “Diurnal rhythms in Metabolism: A Day in The life of a Unicellular, Diazotrophic Cyanobacterium,” Photosynthesis Research, Vol. 58, No. 1, 1998, pp. 25-42. http://dx.doi.org/10.1023/A:1006137605802
[36]
A. Bandyopadhyay, J. Stockel, H. Min, L. A. Sherman and H. B. Pakrasi, “High Rates of Photobiological H2 Production by a Cyanobacterium under Aerobic Conditions,” Nature Communications, Vol. 1, No. 9, 2010, p. 139. http://dx.doi.org/10.1038/ncomms1139
[37]
S. Taikhao, S. Junyapoon, A. Incharoensakdi and S. Phunpruch, “Factors Affecting Biohydrogen Production by Unicellular Halotolerant Cyanobacterium aphanothece Halophytica,” Journal of Applied Phycology, Vol. 25, No. 2, 2013, pp. 575-585.
[38]
D. C. Ducat, G. Sachdeva and P. A. Silver, “Rewiring Hydrogenase-Dependent Redox Circuits in Cyanobacteria,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 10, 2011, pp. 3941-3946. http://dx.doi.org/10.1073/pnas.1016026108
[39]
P. D. Weyman, W. A. Vargas, Y. Tong, J. Yu, P.-C. Maness, H. O. Smith and Q. Xu, “Heterologous Expression of Alteromonas macleodii and Thiocapsa roseopersicina [NiFe] Hydrogenases in Synechococcus elongatus,” PLoS ONE, Vol. 6, No. 5, 2011, Article ID: e20126. http://dx.doi.org/10.1371/journal.pone.0020126
[40]
F. Gutthann, M. Egert, A. Marques and J. Appel, “Inhibition of Respiration and Nitrate Assimilation Enhances Photohydrogen Evolution under Low Oxygen Concentrations in Synechocystis sp. PCC 6803,” Biochimica et Biophysica Acta—Bioenergetics, Vol. 1767, No. 2, 2007, pp. 161-169. http://dx.doi.org/10.1016/j.bbabio.2006.12.003
[41]
G. Ananyev, D. Carrieri and G. C. Dismukes, “Optimization of Metabolic Capacity and Flux Through Environmental Cues to Maximize Hydrogen Production by the Cyanobacterium ‘Arthrospira (Spirulina) Maxima’,” Applied Environmental Microbiology, Vol. 74, No. 19, 2008, pp. 6102-6113. http://dx.doi.org/10.1128/AEM.01078-08
[42]
K. McNeely, Y. Xu, N. Bennette, D. A. Bryant and G. C. Dismukes, “Redirecting Reductant Flux into Hydrogen Production via Metabolic Engineering of Fermentative Carbon Metabolism in a Cyanobacterium,” Applied Environmental Microbiology, Vol. 76, No. 15, 2010, pp. 5032-5038. http://dx.doi.org/10.1128/AEM.00862-10
[43]
A. J. McCormick, P. Bombelli, D. J. Lea-Smith, R. W. Bradley, A. M. Scott, A. C. Fisher, A. G. Smith and C. J. Howe, “Hydrogen Production Through Oxygenic Photosynthesis Using the Cyanobacterium Synechocystis sp. PCC 6803 in a Bio-Photoelectrolysis Cell (BPE) System,” Energy and Environmental Science, Vol. 6, No. 9, pp. 2682-2690. http://dx.doi.org/10.1039/c3ee40491a
[44]
A. Badura, D. Guschin, T. Kothe, M. J. Kopczak, W. Schuhmann and M. Rogner, “Photocurrent Generation by Photosystem 1 Integrated in Crosslinked Redox Hydrogels,” Energy and Environmental Science, Vol. 4, No. 7, 2011, pp. 2435-2440. http://dx.doi.org/10.1039/c1ee01126j
[45]
R. Grimme, C. E. Lubner, D. A. Bryant and J. H. Golbeck, “Photosystem I/Molecular Wire/Metal Nanoparticle Bioconjugates for the Photocatalytic Production of H2,” Journal of the American Chemical Society, Vol. 130, No. 20, 2008, pp. 6308-6309. http://dx.doi.org/10.1021/ja800923y
[46]
C. E. Lubner, R. Grimme, D. A. Bryant and J. H. Golbeck, “Wiring Photosystem I for Direct Solar Hydrogen Production,” Biochemistry, Vol. 49, No. 3, 2010, pp. 404-414. http://dx.doi.org/10.1021/bi901704v
[47]
A. Badura, T. Kothe, W. Schuhmann and M. Rogner, “Wiring Photosynthetic Enzymes to Electrodes,” Energy and Environmental Science, Vol. 4, No. 9, 2011, 3263-3274. http://dx.doi.org/10.1039/c1ee01285a
[48]
I. Iwuchukwu, M. Vaughn, N. Myers, H. O’Neill, P. Frymier and B. D. Bruce, “Self-Organized Photosynthetic Nanoparticle for Cell-Free Hydrogen Production,” Nature Nanotechnology, Vol. 5, No. 1, 2010, pp. 73-79. http://dx.doi.org/10.1038/nnano.2009.315
[49]
M. Ihara, H. Nishihara, K.-S. Yoon, O. Lenz, B. Friedrich, H. Nakamoto, K. Kojima, D. Honma, T. Kamachi and I. Okura, “Light-Driven Hydrogen Production by a Hybrid Complex of a [NiFe]-Hydrogenase and the Cyanobacterial Photosystem I,” Photochemistry and Photobiology, Vol. 82, No. 3, 2006, pp. 676-682. http://dx.doi.org/10.1562/2006-01-16-RA-778
[50]
H. Krassen, A. Schwarze, B. Friedrich, K. Ataka, O. Lenz and J. Heberle, “Photosynthetic Hydrogen Production by a Hybrid Complex of Photosystem I and [NiFe]-Hydrogenase,” ACS Nano, Vol. 3, No. 12, 2009, pp. 4055-4061. http://dx.doi.org/10.1021/nn900748j
[51]
C. E. Lubner, P. Knorzer, P. J. N. Silva, K. A. Vincent, T. Happe, D. A. Bryant and J. H. Golbeck, “Wiring an [FeFe]-Hydrogenase with Photosystem I for Light-Induced Hydrogen Production,” Biochemistry, Vol. 49, No. 48, 2010, pp. 10264-10266.
[52]
J. Maly, J. Krejci, M. Ilie, L. Jacubka, J. Masojidek, R. Pilloton, K, Sameh, P. Steffan, Z. Stryhal and M. Sugiura, “Monolayers of photosystem II on Gold Electrodes with Enhanced Sensor Response—Effect of Porosity and Protein Layer Arrangement,” Analytical and Bioanalytical Chemistry, Vol. 381, No. 8, 2005, pp. 1558-1567. http://dx.doi.org/10.1007/s00216-005-3149-9
[53]
J. Maly, J. Masojidek, A. Masci, M. Ilie, E. Cianci, V. Foglietti, W. Vastarella and R. Pilloton, “Direct Mediatorless Electron Transport Between the Monolayer of Photosystem II and Poly (Mercapto-p-Benzoquinone) Modified Gold Electrode—New Design of Biosensor for Herbicide Detection,” Biosensors and Bioelectronics, Vol. 21, No. 6, 2005, pp. 923-932. http://dx.doi.org/10.1016/j.bios.2005.02.013
[54]
A. Badura, B. Esper, K. Ataka, C. Grunwald, C. Woll, J. Kuhlmann, J. Heberle and M. Rogner, “Light-Driven Water Splitting for (Bio-)Hydrogen Production: Photosystem 2 as the Central Part of a Bioelectrochemical Device,” Photochemistry and Photobiology, Vol. 82, No. 5, 2006, pp. 1385-1390. http://dx.doi.org/10.1562/2006-07-14-RC-969
[55]
A. Badura, D. Guschin, B. Esper, T. Kothe, S. Neugebauer, W. Schuhmann and M. Rogner, “Photo-Induced Electron Transfer Between Photosystem 2 via Crosslinked Redox Hydrogels,” Electroanalysis, Vol. 20, No. 10, 2008, pp. 1043-1047. http://dx.doi.org/10.1002/elan.200804191
