Elimination of Rubisco alters the regulation of nitrogenase activity and increases hydrogen production in Rhodospirillum rubrum

International Journal of Hydrogen Energy

Volumn 35, Issue 14, 2010, Pages 7377-7385

  Wang, Di ^a,b   Zhang, Yaoping ^a,b   Welch, Emily ^b   Li, Jilun ^a   Roberts, Gary P ^b  

^a College of Biological Sciences   (China)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

H2 production; NifA; Nitrogenase; Rhodospirillum rubrum; Rubisco

Indexed keywords

ANAEROBIC CONDITIONS; ATMOSPHERIC NITROGEN; BIOLOGICAL PRODUCTION; CONSTITUTIVELY ACTIVES; LIMITING CONDITION; LONGER TIME FRAMES; NITROGENASE; NITROGENASE ACTIVITY; PHOTOSYNTHETIC BACTERIAS; POSTTRANSLATIONAL REGULATION; RECOMBINANT STRAINS; REDUCTANTS; RHODOSPIRILLUM RUBRUM; RUBISCO; TRANSCRIPTIONAL ACTIVATORS; WILD TYPES;

AMMONIUM COMPOUNDS; BACTERIA; HYDROGEN PRODUCTION; NITROGEN;

NITROGEN FIXATION;

EID: 77953913698     PISSN: 03603199     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijhydene.2010.04.183     Document Type: Article

References (61)

1. Singh S.P., Srivastava S.C., and Pandey K.D. Hydrogen-production by Rhodopseudomonas at the expense of vegetable starch, sugarcane juice and whey. Int J Hydrogen Energy 19 (1994) 437-440
2. Ike A., Murakawa T., Kawaguchi H., Hirata K., and Miyamoto K. Photoproduction of hydrogen from raw starch using a halophilic bacterial community. J Biosci Bioeng 88 (1999) 72-77
3. Fang H.H.P., Liu H., and Zhang T. Phototrophic hydrogen production from acetate and butyrate in wastewater. Int J Hydrogen Energy 30 (2005) 785-793
4. Franchi E., Tosi C., Scolla G., Penna G.D., Rodriguez F., and Pedroni P.M. Metabolically engineered Rhodobacter sphaeroides RV strains for improved biohydrogen photoproduction combined with disposal of food wastes. Mar Biotechnol 6 (2004) 552-565
5. 2 photoproduction by Rhodospirillum rubrum. Appl Microbiol Biotechnol 37 (1992) 496-500
6. Akköse S., Gündüz U., Yücel M., and Eroǧlu I. Effects of ammonium ion, acetate and aerobic conditions on hydrogen production and expression levels of nitrogenase genes in Rhodobacter sphaeroides O.U.001. Int J Hydrogen Energy 34 (2009) 8818-8827
7. Jamil Z., Annuar M.S.M., Ibrahim S., and Vikineswary S. Optimization of phototrophic hydrogen production by Rhodopseudomonas palustris PBUM001 via statistical experimental design. Int J Hydrogen Energy 34 (2009) 7502-7512
8. Melnicki M.R., Eroglu E., and Melis A. Changes in hydrogen production and polymer accumulation upon sulfur-deprivation in purple photosynthetic bacteria. Int J Hydrogen Energy 34 (2009) 6157-6170
9. Melnicki M.R., Bianchi L., De Philippis R., and Melis A. Hydrogen production during stationary phase in purple photosynthetic bacteria. Int J Hydrogen Energy 33 (2008) 6525-6534
10. +. Int J Hydrogen Energy 26 (2001) 1149-1154
11. Nath K., Kumar A., and Das D. Hydrogen production by Rhodobacter sphaeroides strain O.U.001 using spent media of Enterobacter cloacae strain DM11. Appl Microbiol Biotechnol 68 (2005) 533-541
12. Xie G.J., Feng L.B., Ren N.Q., Ding J., Liu C., Xing D.F., et al. Control strategies for hydrogen production through co-culture of Ethanoligenens harbinense B49 and immobilized Rhodopseudomonas faecalis RLD-53. Int J Hydrogen Energy 35 (2010) 1929-1935
13. Ooshima H., Takakuwa S., Katsuda T., Okuda M., Shirasawa T., Azuma M., et al. Production of hydrogen by a hydrogenase-deficient mutant of Rhodobacter capsulatus. J Ferment Bioeng 85 (1998) 470-475
14. Rey F.E., Oda Y., and Harwood C.S. Regulation of uptake hydrogenase and effects of hydrogen utilization on gene expression in Rhodopseudomonas palustris. J Bacteriol 188 (2006) 6143-6152
15. Zorin N.A., Lissolo T., Colbeau A., and Vignais P.M. Increased hydrogen production by Rhodobacter capsulatus strains deficient in uptake hydrogenase. J Mar Biotechnol 4 (1996) 28-33
16. Kars G., Gündüz U., Rakhely G., Yücel M., Eroǧlu I., and Kovacs K.L. Improved hydrogen production by uptake hydrogenase deficient mutant strain of Rhodobacter sphaeroides O.U.001. Int J Hydrogen Energy 33 (2008) 3056-3060
17. Kim E.J., Kim J.S., Kim M.S., and Lee J.K. Effect of changes in the level of light harvesting complexes of Rhodobacter sphaeroides on the photoheterotrophic production of hydrogen. Int J Hydrogen Energy 31 (2006) 531-538
18. Gest H., Kamen M.D., and Beregoff H.M. Studies on the metabolism of photosynthetic bacteria. V. Photoproduction of hydrogen and nitrogen fixation by Rhodospirillum rubrum. J Biol Chem 182 (1950) 153-170
19. Bonam D., McKenna M.C., Stephens P.J., and Ludden P.W. Nickel-deficient carbon monoxide dehydrogenase from Rhodospirillum rubrum: in vivo and in vitro activation by exogenous nickel. Proc Natl Acad Sci USA 85 (1988) 31-35
20. Fox J.D., Kerby R.L., Roberts G.P., and Ludden P.W. Characterization of the CO-induced, CO-tolerant hydrogenase from Rhodospirillum rubrum and the gene encoding the large subunit of the enzyme. J Bacteriol 178 (1996) 1515-1524
21. Maness P.C., and Weaver P.F. Evidence for three distinct hydrogenase activities in Rhodospirillum rubrum. Appl Microbiol Biotechnol 57 (2001) 751-756
22. Schön G., and Voelskow H. Pyruvate fermentation in Rhodospirillum rubrum and after transfer from aerobic to anaerobic conditions in the dark. Arch Microbiol 107 (1976) 87-92
23. Gorrell T.E., and Uffen R.L. Fermentative metabolism of pyruvate by Rhodospirillum rubrum after anaerobic growth in darkness. J Bacteriol 131 (1977) 533-543
24. 2 production of Rhodospirillum rubrum during adaptation to anaerobic dark conditions. Arch Microbiol 125 (1980) 245-249
25. Kim E.J., Lee M.K., Kim M.S., and Lee J.K. Molecular hydrogen production by nitrogenase of Rhodobacter sphaeroides and by Fe-only hydrogenase of Rhodospirillum rubrum. Int J Hydrogen Energy 33 (2008) 1516-1521
26. Zhu R.Y., Wang D., Zhang Y.P., and Li J.L. Hydrogen production by draTGB hupL double mutant of Rhodospirillum rubrum under different light conditions. Chin Sci Bull 51 (2006) 2611-2618
27. Burris R.H. Nitrogenases. J Biol Chem 266 (1991) 9339-9342
28. Ludden P.W., and Roberts G.P. Regulation of nitrogenase activity by reversible ADP ribosylation. Curr Top Cell Regul 30 (1989) 23-56
29. Nordlund S., and Ludden P.W. Post-translational regulation of nitrogenase in photosynthetic bacteria. In: Klipp W., Masephol B., Gallon J.R., and Newton W.E. (Eds). Genetics and regulation of nitrogen fixation in free-living bacteria (2004), Kluwer Academic Publishers., Dordrecht, The Netherlands 175-196
30. II homologs in the photosynthetic bacterium Rhodospirillum rubrum. Symbiosis 35 (2003) 85-100
31. Zhang Y., Pohlmann E.L., Ludden P.W., and Roberts G.P. Mutagenesis and functional characterization of the glnB, glnA, and nifA genes from the photosynthetic bacterium Rhodospirillum rubrum. J Bacteriol 182 (2000) 983-992
32. Liang J.H., Nielsen G.M., Lies D.P., Burris R.H., Roberts G.P., and Ludden P.W. Mutations in the draT and draG genes of Rhodospirillum rubrum result in loss of regulation of nitrogenase by reversible ADP-ribosylation. J Bacteriol 173 (1991) 6903-6909
33. Zhang Y., Burris R.H., Ludden P.W., and Roberts G.P. Comparison studies of dinitrogenase reductase ADP-ribosyl transferase/dinitrogenase reductase activating glycohydrolase regulatory systems in Rhodospirillum rubrum and Azospirillum brasilense. J Bacteriol 177 (1995) 2354-2359
34. Zou X., Zhu Y., Pohlmann E.L., Li J., Zhang Y., and Roberts G.P. Identification and functional characterization of NifA variants that are independent of GlnB activation in the photosynthetic bacterium Rhodospirillum rubrum. Microbiology 154 (2008) 2689-2699
35. Joshi H.M., and Tabita F.R. A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixation. Proc Natl Acad Sci USA 93 (1996) 14515-14520
36. Tichi M.A., and Tabita F.R. Maintenance and control of redox poise in Rhodobacter capsulatus strains deficient in the Calvin-Benson-Bassham pathway. Arch Microbiol 174 (2000) 322-333
37. Falcone D.L., and Tabita F.R. Expression of endogenous and foreign ribulose 1,5-bisphosphate carboxylase-oxygenase (RubisCO) genes in a RubisCO deletion mutant of Rhodobacter sphaeroides. J Bacteriol 173 (1991) 2099-2108
38. Paoli G.C., Vichivanives P., and Tabita F.R. Physiological control and regulation of the Rhodobacter capsulatus cbb operons. J Bacteriol 180 (1998) 4258-4269
39. 2 fixation in Rhodobacter sphaeroides and evidence that ribulose bisphosphate carboxylase/oxygenase activity serves to maintain the redox balance of the cell. J Bacteriol 175 (1993) 3372-3379
40. 2 fixation gene expression in a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion strain of Rhodospirillum rubrum. J Bacteriol 175 (1993) 5066-5077
41. Fitzmaurice W.P., Saari L.L., Lowery R.G., Ludden P.W., and Roberts G.P. Genes coding for the reversible ADP-ribosylation system of dinitrogenase reductase from Rhodospirillum rubrum. Mol Gen Genet 218 (1989) 340-347
42. Ormerod J.G., Ormerod K.S., and Gest H. Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism. Arch Biochem Biophys 94 (1961) 449-463
43. Lehman L.J., and Roberts G.P. Identification of an alternative nitrogenase system in Rhodospirillum rubrum. J Bacteriol 173 (1991) 5705-5711
44. Zhang Y., Pohlmann E.L., Ludden P.W., and Roberts G.P. Functional characterization of three GlnB homologs in the photosynthetic bacterium Rhodospirillum rubrum: roles in sensing ammonium and energy status. J Bacteriol 183 (2001) 6159-6168
45. Simon R., Priefer U.B., and Pühler A. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1 (1983) 784-791
46. Schweizer H.P. Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15 (1993) 831-834
47. Zhang Y., Burris R.H., Ludden P.W., and Roberts G.P. Posttranslational regulation of nitrogenase activity by anaerobiosis and ammonium in Azospirillum brasilense. J Bacteriol 175 (1993) 6781-6788
48. Hartmann A., Fu H., and Burris R.H. Regulation of nitrogenase activity by ammonium chloride in Azospirillum spp. J Bacteriol 165 (1986) 864-870
49. Lehman L.J., Fitzmaurice W.P., and Roberts G.P. The cloning and functional characterization of the nifH gene of Rhodospirillum rubrum. Gene 95 (1990) 143-147
50. Rey F.E., Heiniger E.K., and Harwood C.S. Redirection of metabolism for biological hydrogen production. Appl Environ Microbiol 73 (2007) 1665-1671
51. Halbleib C.M., Zhang Y., and Ludden P.W. Regulation of dinitrogenase reductase ADP-ribosyltransferase and dinitrogenase reductase-activating glycohydrolase by a redox-dependent conformational change of nitrogenase Fe protein. J Biol Chem 275 (2000) 3493-3500
52. Halbleib C.M., Zhang Y., Roberts G.P., and Ludden P.W. Effects of perturbations of the nitrogenase electron transfer chain on reversible ADP-ribosylation of nitrogenase Fe protein in Klebsiella pneumoniae strains bearing the Rhodospirillum rubrum dra operon. J Bacteriol 182 (2000) 3681-3687
53. Thorneley R.N., and Lowe D.J. Nitrogenase of Klebsiella pneumoniae. Kinetics of the dissociation of oxidized iron protein from molybdenum-iron protein: identification of the rate-limiting step for substrate reduction. Biochem J 215 (1983) 393-403
54. Zhang Y., Pohlmann E.L., and Roberts G.P. Effect of perturbation of ATP level on the activity and regulation of nitrogenase in Rhodospirillum rubrum. J Bacteriol 191 (2009) 5526-5537
55. Kim E.J., Kim M.S., and Lee J.K. Hydrogen evolution under photoheterotrophic and dark fermentative conditions by recombinant Rhodobacter sphaeroides containing the genes for fermentative pyruvate metabolism of Rhodospirillum rubrum. Int J Hydrogen Energy 33 (2008) 5131-5136
56. 2 production by Rhodobacter capsulatus upon interposon mutagenesis in the hupL gene. Appl Microbiol Biotechnol 40 (1994) 687-690
57. 2 photoproduction by hup mutants of Rhodospirillum rubrum. Appl Environ Microbiol 60 (1994) 1768-1774
58. Kars G., Gündüz U., Yücel M., Rakhely G., and Kovacs K.L. Eroǧlu I. Evaluation of hydrogen production by Rhodobacter sphaeroides O.U.001 and its hupSL deficient mutant using acetate and malate as carbon sources. Int J Hydrogen Energy 34 (2009) 2184-2190
59. Öztürk Y., Yücel M., Daldal F., Mandaci{dotless} S., Gündüz U., Türker L., et al. Hydrogen production by using Rhodobacter capsulatus mutants with genetically modified electron transfer chains. Int J Hydrogen Energy 31 (2006) 1545-1552
60. Kanemoto R.H., and Ludden P.W. Effect of ammonia, darkness, and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification in Rhodospirillum rubrum. J Bacteriol 158 (1984) 713-720
61. Liu J., Ding Y., Jiang W., Tian J., Li Y., and Li J. A mutation upstream of an ATPase gene significantly increases magnetosome production in Magnetospirillum gryphiswaldense. Appl Microbiol Biotechnol 81 (2008) 551-558