The role of the bidirectional hydrogenase in cyanobacteria

Bioresource Technology

Volumn 102, Issue 18, 2011, Pages 8368-8377

  Carrieri, Damian ^a   Wawrousek, Karen ^a   Eckert, Carrie ^a   Yu, Jianping ^a   Maness, Pin Ching ^a  

^a NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

Bidirectional hydrogenase; Cyanobacteria; Hox hydrogenase; Hydrogen; Hydrogenase

Indexed keywords

CYANOBACTERIA; HOX HYDROGENASE; HYDROGEN GAS; HYDROGENASES; RENEWABLE FUELS;

ENZYMES; HYDROGEN; PHYSIOLOGY; SOLAR ENERGY;

SOLAR POWER GENERATION;

BACTERIAL ENZYME; BIOFUEL; FOSSIL FUEL; HOX PROTEIN; HYDROGEN; HYDROGENASE; IRON; NITROGEN; NITROGENASE;

CYANOBACTERIUM; ENZYME ACTIVITY; METABOLISM; OXIDATION; PHYSIOLOGICAL RESPONSE; REDUCTION; RENEWABLE RESOURCE; SOLAR POWER;

ARTICLE; CYANOBACTERIUM; GENETIC CODE; HYDROPOWER; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; SOLAR ENERGY;

BIOCATALYSIS; CYANOBACTERIA; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGENASE; MODELS, BIOLOGICAL; PHYLOGENY;

CYANOBACTERIA;

EID: 80051681335     PISSN: 09608524     EISSN: 18732976     Source Type: Journal    
DOI: 10.1016/j.biortech.2011.03.103     Document Type: Article

References (74)

1. Agervald A., Baebprasert W., Zhang X., Incharoensakdi A., Lindblad P., Stensjö K. The CyAbrB transcription factor CalA regulates the iron superoxide dismutase in Nostoc sp. strain PCC 7120. Environ. Microbiol. 2010, 12:2826-2837.
2. Agervald A., Zhang X.H., Stensjo K., Devine E., Lindblad P. CalA, a cyanobacterial AbrB protein, interacts with the upstream region of hypC and acts as a repressor of its transcription in the cyanobacterium Nostoc sp strain PCC 7120. Appl. Environ. Microbiol. 2010, 76:880-890.
3. Ananyev G., Carrieri D., Dismukes G.C. Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the cyanobacterium " Arthrospira (Spirulina) maxima" Appl. Environ. Microbiol. 2008, 74:6102-6113.
4. Antal T.K., Oliveira P., Lindblad P. The bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. Int. J. Hydrogen Energ. 2006, 31:1439-1444.
5. Appel J., Schulz R. Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising?. J. Photochem. Photobiol. B 1998, 47:1-11.
6. Appel J., Phunpruch S., Steinmuller K., Schulz R. The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch. Microbiol. 2000, 173:333-338.
7. Axelsson R., Lindblad P. Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel. Appl. Environ. Microbiol. 2002, 68:444-447.
8. Axelsson R., Oxelfelt F., Lindblad P. Transcriptional regulation of Nostoc uptake hydrogenase. Fems. Microbiol. Lett. 1999, 170:77-81.
9. Barz M., Beimgraben C., Staller T., Germer F., Opitz F., Marquardt C., Schwarz C., Gutekunst K., Vanselow K.H., Schmitz R., LaRoche J., Schulz R., Appel J. Distribution analysis of hydrogenases in surface waters of marine and freshwater environments. PLoS ONE 2010, 5:e13846.
10. Blokesch M., Bock A. Maturation of [NiFe]-hydrogenases in Escherichia coli: the HypC cycle. J. Mol. Biol. 2002, 324:287-296.
11. Blokesch M., Paschos A., Bauer A., Reissmann S., Drapal N., Bock A. Analysis of the transcarbamoylation-dehydration reaction catalyzed by the hydrogenase maturation proteins HypF and HypE. Eur. J. Biochem. 2004, 271:3428-3436.
12. Blokesch M., Rohrmoser M., Rode S., Bock A. HybF, a zinc-containing protein involved in NiFe hydrogenase maturation. J. Bacteriol. 2004, 186:2603-2611.
13. Boison G., Bothe H., Schmitz O. Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR. Curr. Microbiol. 2000, 40:315-321.
14. Brentner L.B., Peccia J., Zimmerman J.B. Challenges in developing biohydrogen as a sustainable energy source. Implications for a research agenda. Environ. Sci. Technol. 2010, 44:2243-2254.
15. Carrieri D., Momot D., Brasg I.A., Ananyev G., Lenz O., Bryant D.A., Dismukes G.C. Boosting autofermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl. Environ. Microbiol. 2010, 76:6455-6462.
16. Cournac L., Mus F., Bernard L., Guedeney G., Vignais P., Peltier G. Limiting steps of hydrogen production in Chlamydomonas reinhardtii and Synechocystis PCC 6803 as analysed by light-induced gas exchange transients. Int. J. Hydrogen Energ. 2002, 27:1229-1237.
17. Cournac L., Guedeney G., Peltier G., Vignais P.M. Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. J. Bacteriol. 2004, 186:1737-1746.
18. Domain F., Houot L., Chauvat F., Cassier-Chauvat C. Function and regulation of the cyanobacterial genes lexA, recA and ruvB: LexA is critical to the survival of cells facing inorganic carbon starvation. Mol. Microbiol. 2004, 53:65-80.
19. Drapal N., Maier T.H.P., Bock A. Nickel incorporation into nickel-dependent enzymes. Period. Biol. 1998, 100:45-51.
20. Dutta D., De D., Chaudhuri S., Bhattacharya S.K. Hydrogen production by cyanobacteria. Microb. Cell Fact. 2005, 4:36.
21. Emerson S., Stump C., Johnson B., Karl D.M. In situ determination of oxygen and nitrogen dynamics in the upper ocean. Deep Sea Research Part I: Oceanographic Research Papers 2002, 49:941-952.
22. Germer F., Zebger I., Saggu M., Lendzian F., Schulz R., Appel J. Overexpression, isolation, spectroscopic characterization of the bidirectional [NiFe] hydrogenase from Synechocystis sp. PCC 6803. J. Biol. Chem. 2009, 284:36462-36472.
23. Ghirardi M.L., Posewitz M.C., Maness P.C., Dubini A., Seibert M. Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu. Rev. Plant Biol. 2007, 58:71-91.
24. Ghirardi M.L., Dubini A., Yu J., Maness P.C. Photobiological hydrogen-producing systems. Chem. Soc. Rev. 2009, 38:52-61.
25. Goris, T., Wait, A.F., Saggu, M., Fritsch, J., Heidary, N., Stein, M., Zebger, I., Lendzian, F., Armstrong, F.A., Friedrich, B., Lenz, O., 2011. A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nat. Chem. Biol. doi:10.1038/nchembio.555.
26. Gutekunst K., Phunpruch S., Schwarz C., Schuchardt S., Schulz-Friedrich R., Appel J. LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol. Microbiol. 2005, 58:810-823.
27. Gutthann F., Egert M., Marques A., Appel J. Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. BBA-Bioenergetics 2007, 1767:161-169.
28. Happe R.P., Roseboom W., Pierik A.J., Albracht S.P.J., Bagley K.A. Biological activation of hydrogen. Nature 1997, 385:126.
29. Hoffmann D., Gutekunst K., Klissenbauer M., Schulz-Friedrich R., Appel J. Mutagenesis of hydrogenase accessory genes of Synechocystis sp. PCC 6803-Additional homologues of hypA and hypB are not active in hydrogenase maturation. FEBS J. 2006, 273:4516-4527.
30. Howitt C.A., Vermaas W.F.J. 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. The Phototrophic Prokaryotes 1999, 595-601. Kluwer Academic/Plenum Publishers, New York, NY USA. G.A. Peschek, W. Löffelhardt, G. Schmetterer (Eds.).
31. Hube M., Blokesch M., Bock A. Network of hydrogenase maturation in Escherichia coli: role of accessory proteins HypA and HybF. J. Bacteriol. 2002, 184:3879-3885.
32. Ito H., Mutsuda M., Murayama Y., Tomita J., Hosokawa N., Terauchi K., Sugita C., Sugita M., Kondo T., Iwasaki H. Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc. Natl. Acad. Sci. USA 2009, 106:14168-14173.
33. James, B.D., Baum, G.N., Perez, J., Baum, K.N., 2009. Technoeconomic Boundary Analysis of Biological Pathways to Hydrogen Production. N.R.E. Laboratory, Directed Technologies, Inc., contract number: NREL/SR-560-46674: http://www.eere.energy.gov/hydrogenandfuelcells/pdfs/46674.pdf.
34. Kentemich T., Bahnweg M., Mayer F., Bothe H. Localization of the reversible hydrogenase in cyanobacteria. Z. Naturforsch. 1989, 44:384-391.
35. Kiss E., Kos P.B., Vass I. Transcriptional regulation of the bidirectional hydrogenase in the cyanobacterium Synechocystis 6803. J. Biotechnol. 2009, 142:31-37.
36. Kosourov S.N., Seibert M. Hydrogen photoproduction by nutrient-deprived Chlamydomonas reinhardtii cells immobilized within thin alginate films under aerobic and anaerobic conditions. Biotechnol. Bioeng. 2009, 102:50-58.
37. Kucho K., Okamoto K., Tsuchiya Y., Nomura S., Nango M., Kanehisa M., Ishiura M. Global analysis of circadian expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 2005, 187:2190-2199.
38. Lee H.-S., Vermaas W.F.J., Rittmann B.E. Biological hydrogen production: prospects and challenges. Trends Biotechnol. 2010, 28:262-271.
39. Li S., Xu M., Su Z. Computational analysis of LexA regulons in cyanobacteria. BMC Genom. 2010, 11:527.
40. Liebgott P.-P., Leroux F., Burlat B., Dementin S., Baffert C., Lautier T., Fourmond V., Ceccaldi P., Cavazza C., Meynial-Salles I., Soucaille P., Fontecilla-Camps J.C., Guigliarelli B., Bertrand P., Rousset M., Leger C. Relating diffusion along the substrate tunnel and oxygen sensitivity in hydrogenase. Nat. Chem. Biol. 2010, 6:63-70.
41. Lieman-Hurwitz J., Haimovich M., Shalev-Malul G., Ishii A., Hihara Y., Gaathon A., Lebendiker M., Kaplan A. A cyanobacterial AbrB-like protein affects the apparent photosynthetic affinity for CO2 by modulating low-CO2-induced gene expression. Environ. Microbiol. 2009, 11:927-936.
42. Long M., Liu J., Chen Z., Bleijlevens B., Roseboom W., Albracht S. Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module. J. Biol. Inorg. Chem. 2007, 12:62-78.
43. Ludwig M., Schulz-Friedrich R., Appel J. Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: implications for the phylogenetic origin of cyanobacterial and algal hydrogenases. J. Mol. Evol. 2006, 63:758-768.
44. Magalon A., Bock A. Analysis of the HypC-HycE complex, a key intermediate in the assembly of the metal center of the Escherichia coli hydrogenase 3. J. Biol. Chem. 2000, 275:21114-21120.
45. Maier T., Jacobi A., Sauter M., Bock A. The product of the HypB Gene, which is required for nickel incorporation into hydrogenase, is a novel guanine nucleotide-binding protein. J. Bacteriol. 1993, 175:630-635.
46. Maier T., Lottspeich F., Bock A. GTP-hydrolysis by HypB is essential for nickel insertion into hydrogenases of Escherichia coli. Eur. J. Biochem. 1995, 230:133-138.
47. Massanz C., Schmidt S., Friedrich B. Subforms and in vitro reconstitution of the NAD-reducing hydrogenase of Alcaligenes eutrophus. J. Bacteriol. 1998, 180:1023-1029.
48. McKinlay J.B., Harwood C.S. Photobiological production of hydrogen gas as a biofuel. Curr. Opin. Microgiol. 2010, 21:244-251.
49. McNeely K., Xu Y., Bennette N., Bryant D.A., Dismukes G.C. Redirecting reductant flux into hydrogen production via metabolic engineering of fermentative carbon metabolism in a cyanobacterium. Appl. Environ. Microbiol. 2010, 76:5032-5038.
50. McNeely K., Xu Y., Ananyev G., Bennette N., Bryant D.A., Dismukes G.C. Synechococcus sp. strain PCC 7002 nifJ mutant lacking pyruvate: ferredoxin oxidoreductase. Appl. Environ. Microbiol. 2011, 77:2435-2444.
51. Moezelaar R., Bijvank S.M., Stal L.J. Fermentation and sulfur reduction in the mat-building cyanobacterium Microcoleus chthonoplastes. Appl. Environ. Microbiol. 1996, 62:1752-1758.
52. Oliveira P., Lindblad P. LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. Fems. Microbiol. Lett. 2005, 251:59-66.
53. Oliveira P., Lindblad P. An AbrB-like protein regulates the expression of the bidirectional hydrogenase in Synechocystis sp. strain PCC 6803. J. Bacteriol. 2008, 190:1011-1019.
54. Peschek G.A., Obinger C., Paumann M. The respiratory chain of blue-green algae (cyanobacteria). Physiol. Plantarum 2004, 120:358-369.
55. Pierik A.J., Roseboom W., Happe R.P., Bagley K.A., Albracht S.P.J. Carbon monoxide and cyanide as intrinsic ligands to iron in the active site of [NiFe]-hydrogenases. J. Biol. Chem. 1999, 274:3331-3337.
56. Pinto F.A.L., Troshina O., Lindblad P. A brief look at three decades of research on cyanobacterial hydrogen evolution. Int. J. Hydrogen Energ. 2002, 27:1209-1215.
57. Prince R.C., Kheshgi H.S. The photobiological production of hydrogen: potential efficiency and effectiveness as a renewable fuel. Crit. Rev. Microbiol. 2005, 31:19-31.
58. Reissmann S., Hochleitner E., Wang H.F., Paschos A., Lottspeich F., Glass R.S., Bock A. Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands. Science 2003, 299:1067-1070.
59. Schaferjohann J., Bednarski R., Bowien B. Regulation of CO2 assimilation in Ralstonia eutropha: premature transcription termination within the cbb operon. J. Bacteriol. 1996, 178:6714-6719.
60. Schmitz O., Boison G., Salzmann H., Bothe H., Schutz K., Wang S.H., Happe T. HoxE-a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. BBA-Bioenergetics 2002, 1554:66-74.
61. Seibert M., King P.W., Posewitz M.C., Melis A., Ghirardi M.L. Photosynthetic water-splitting for hydrogen production. Bioenergy 2008, 273-291. ASM Press, Washington DC, USA. J.D. Wall, C.S. Harwood, A. Demain (Eds.).
62. Serebriakova L., Zorin N.A., Lindblad P. Reversible hydrogenase in Anabaena variabilis ATCC 29413. Arch. Microbiol. 1994, 161:140-144.
63. Serebryakova L.T., Tsygankov A.A. Two-stage system for hydrogen production by immobilized cyanobacterium Gloeocapsa alpicola CALU 743. Biotechnol. Progr. 2007, 23:1106-1110.
64. Sjoholm J., Oliveira P., Lindblad P. Transcription, regulation of the bidirectional hydrogenase in the cyanobacterium Nostoc sp. strain PCC 7120. Appl. Environ. Microbiol. 2007, 73:5435-5446.
65. Stal L.J., Moezelaar R. Fermentation in cyanobacteria. Fems. Microbiol. Rev. 1997, 21:179-211.
66. Summerfield T.C., Toepel J.r., Sherman L.A. Low-oxygen induction of normally Cryptic psbA genes in cyanobacteria. Biochemistry-US 2008, 47:12939-12941.
67. Tamagnini P., Costa J.L., Almeida L., Oliveira M.J., Salema R., Lindblad P. Diversity of cyanobacterial hydrogenases, a molecular approach. Curr. Microbiol. 2000, 40:356-361.
68. Tamagnini P., Leitao E., Oliveira P., Ferreira D., Pinto F., Harris D.J., Heidorn T., Lindblad P. Cyanobacterial hydrogenases: diversity, regulation and applications. Fems. Microbiol. Rev. 2007, 31:692-720.
69. Theodoratou E., Paschos A., Magalon A., Fritsche E., Huber R., Bock A. Nickel serves as a substrate recognition motif for the endopeptidase involved in hydrogenase maturation. Eur. J. Biochem. 2000, 267:1995-1999.
70. Troshina O., Serebryakova L., Sheremetieva M., Lindblad P. Production of H-2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. Int. J. Hydrogen Energ. 2002, 27:1283-1289.
71. Tsygankov A. Nitrogen-fixing cyanobacteria: a review. Appl. Biochem. Microbiol. 2007, 43:250-259.
72. Ungerer J.L., Pratte B.S., Thiel T. RNA processing of nitrogenase transcripts in the cyanobacterium Anabaena variabilis. J. Bacteriol. 2010, 192:3311-3320.
73. Vanderoost J., Bulthuis B.A., Feitz S., Krab K., Kraayenhof R. Fermentation metabolism of the unicellular cyanobacterium Cyanothece PCC 7822. Arch. Microbiol. 1989, 152:415-419.
74. Waugh R., Boxer D.H. Pleiotrophic hydrogenase mutants of Escherichia coli K-12: growth in the presence of nickel can restore hydrogenase activity. Biochimie 1986, 68:157-166.