The biochemistry of vitreoscilla hemoglobin

Computational and Structural Biotechnology Journal

Volumn 3, Issue 4, 2012, Pages e201210002-

  Stark, Benjamin C ^a   Dikshit, Kanak L ^b   Pagilla, Krishna R ^a  

^a Illinois Institute of Technology   (United States)

^b INSTITUTE OF MICROBIAL TECHNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84902213849     PISSN: None     EISSN: 20010370     Source Type: Journal    
DOI: 10.5936/csbj.201210002     Document Type: Review

References (73)

1. Webster DA, Hackett DP (1966) The purification and properties of cytochrome o from Vitreoscilla. J Biol Chem 241: 3308-3315.
2. Appleby CA (1969) Electron transport systems of Rhizobium japonicum. II. Rhizobium haemoglobin, cytochromes and oxidases in free-living (cultured) cells. Biochim Biophys Acta 172: 88-105.
3. Wakabayashi S, Matsubara H, Webster DA (1986) Primary sequence of a dimeric bacterial hemoglobin from Vitreoscilla. Nature 322: 481-483. (Pubitemid 16034023)
4. Tarricone C, Galizzi A, Coda A, Ascenzi P, Bolognesi M (1997) Unusual structure of the oxygen-binding site in the dimeric bacterial hemoglobin from Vitreoscilla sp. Structure 5: 497-507. (Pubitemid 27191226)
5. Frey AD, Kallio PT (2003) Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiol Rev 27: 525-45. (Pubitemid 37205168)
6. Vuletich DA, Lecomte TJ (2006) A phylogenetic and structural analysis of truncated hemoglobins. J Molec Evol 62: 196-210.
7. Wittenberg JB, Bolognesi M, Wittenberg BA, Guertin M (2002) Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277: 871-874. (Pubitemid 34968827)
8. Frey AD, Shepherd M, Jokipii-Lukkari S, Haggman H, Kallio PT (2011) The single-domain globin of Vitreoscilla: augmentation of aerobic metabolism for biotechnological applications. Adv Microbiol Physiol 58: 81-139.
9. Freitas TAK, Hou S, Dioum EM, Saito JA, Newhouse J, Gonzalez G, Gilles-Gonzalez M-A, Alam M (2004) Ancestral hemoglobins in Archaea. Proc Nad Acad Sci USA 101: 6675-6680. (Pubitemid 38586033)
10. Gardner PR, Gardner AM, Martin LA, Salzman AL (1998) Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc Nad Acad Sci USA 95: 10378-10383. (Pubitemid 28413075)
11. Hausladen A, Gow AJ, Stamler JS (1998) Nitrosative stress: metabolic pathway involving the flavohemoglobin. Proc Nad Acad Sci USA 95: 14100-14105. (Pubitemid 28549327)
12. Gupta S, Pawaria S, Lu C, Hade MD, Singh C, Yeh SR, Dikshit KL (2012) An unconventional hexacoordinated flavohemoglobin from Mycobacterium tuberculosis. J Biol Chem. 287: 16435-16446.
13. Ramandeep, Hwang KW, Raje M, Kim KJ, Stark BC, Dikshit KL, Webster DA (2001) Vitreoscilla hemoglobin: intracellular localization and binding to membranes. J Biol Chem 276: 24781-24789.
14. Park KW, Kim KJ, Howard AJ, Stark BC, Webster DA (2002) Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases. J Biol Chem 277: 33334-33337. (Pubitemid 34984855)
15. Duk BT (2007) Exploration of protein-protein interactions between Vitreoscilla hemoglobin (VHb) and E. coli Fnr, OxyR and CydA. PhD thesis, Illinois Institute of Technology, Chicago IL USA.
16. Boerman SJ, Webster DA (1982) Control of heme content in Vitreoscilla by oxygen. J Gen Appl Microbiol 28: 35-43. (Pubitemid 12057712)
17. Dikshit KL, Dikshit RP, Webster DA (1990) Study of Vitreoscilla globin (vgb) gene expression and promoter activity in E. coli through transcriptional fusion. Nucl Acids Res 18: 4149-4155.
18. Pringsheim EG (1951) The Vitreoscillaceae: a family of colourless, gliding, filamentous organisms. J Gen Microbiol 5: 124-149.
19. Lin JM, Stark BC, Webster DA (2003) Effects of Vitreoscilla hemoglobin on the 2,4-dinitrotoluene (DNT) dioxygenase activity of Burkholderia and on DNT degradation in two-phase bioreactors. J Ind Microbiol Biotechnol 30: 362-368. (Pubitemid 37041317)
20. Kaur R, Pathania R, Sharma V, Mande SC, Dikshit KL (2002) Chimeric Vitreoscilla hemoglobin (VHb) carrying a flavoreductase domain relieves nitrosative stress in Eschericbia coli: new insight into the functional role of VHb. Appl Environ Microbiol 68: 152-160. (Pubitemid 34031174)
21. Anand AB, Duk T, Singh S, Akbas MY, Webster DA, Stark BC, Dikshit KL (2010) Redox mediated interactions of Vitreoscilla hemoglobin [VHb] with OxyR: novel regulation of VHb biosynthesis under oxidative stress. Biochem J 426: 271-280.
22. Roos V, Andersson CI, Biilow L (2004) Gene expression profiling of Escherichia coli expressing double Vitreoscilla haemoglobin. J Biotechnol 114: 107-120. (Pubitemid 39298289)
23. Dikshit KL, Webster DA (1988) Cloning, characterization and expression of the bacterial globin gene from Vitreoscilla in Escherichia coli. Gene 70: 377-386.
24. Khosla C, Bailey JE (1988) Heterologous expression of a bacterial hemoglobin improves the growth properties of recombinant Escherichia coli. Nature 331: 633-635. (Pubitemid 18049530)
25. Khosravi M, Webster DA, Stark BC (1990) Presence of the bacterial hemoglobin gene improves alpha-amylase production of a recombinant E. coli strain. Plasmid 24: 190-194.
26. Zhang L, Li Y, Wang Z, Xia Y, Chen W, Tang K (2007) Recent developments and future prospects of Vitreoscilla hemoglobin applications in metabolic engineering. Biotechnol Adv 25: 123-136. (Pubitemid 46164798)
27. Stark BC, Dikshit KL, Pagilla KR (2011) Recent advances in understanding the structure, function, and biotechnological usefulness of the hemoglobin from the bacterium Vitreoscilla. Biotechnol Lett 33: 1705-1714.
28. Webster DA (1987) Structure and function of bacterial hemoglobin and related proteins. In: Eichorn GC, Marzilli LG, editors. Advances in inorganic biochemistry, Vol. 7. New York: Elsevier. pp. 245-265.
29. Khosla C, Bailey JE (1989) Evidence for partial export of Vitreoscilla hemoglobin into the periplasmic space in Escherichia coli: Implications for protein function. J Mol Biol 210: 79-89. (Pubitemid 19286589)
30. Tsai PS, Nageli M, Bailey JE (1996) Intracellular expression of Vitreoscilla hemoglobin modifies microaerobic Escherichia coli metabolism through elevated concentration and specific activity of cytochrome o. Biotechnol Bioengin 49: 151-160. (Pubitemid 26011768)
31. Dikshit KL, Orii Y, Navani N, Patel S, Huang H-Y, Stark BC, Webster DA (1998) Site-directed mutagenesis of bacterial hemoglobin: the role of glutamine (E7) in oxygen-binding in the distal heme pocket. Arch Biochem Biophys 349: 161-166. (Pubitemid 28368402)
32. Orii Y, Webster DA (1986) Photodissociation of oxygenated cytochrome o(s) (Vitreoscilla) and kinetic studies of reassociation. J Biol Chem 261: 3544-3547.
33. Verma S, Patel S, Kaur R, Chung YT, Duk BT, Dikshit KL, Stark BC, Webster DA (2005) Mutational study of the bacterial hemoglobin distal heme pocket. Biochem Biophys Res Commun 326: 290-297. (Pubitemid 39593545)
34. Kaur R, Ahuja S, Anand A, Singh B, Stark BC, Webster DA, Dikshit KL (2008) Functional implications of the proximal site hydrogen bonding network in Vitreoscilla hemoglobin (VHb): role of Tyr95(G5) and Tyr 126(HI2). FEBS Lett 582: 2494-3500.
35. Lee SY, Stark BC, Webster DA (2004) Structure-function of the Vitreoscilla hemoglobin D-region. Biochem Biophys Res Comm 316: 1101-1106.
36. Dikshit RP, Dikshit KL, Liu XY, Webster DA (1992) The bacterial hemoglobin from Vitreoscilla can support the aerobic growth of Escherichia coli lacking terminal oxidases. Arch Biochem Biophys 293: 241-245.
37. Gonzales-Prevatt V, Webster DA (1980) Purification and properties of NADH cytochrome o reductase from Vitreoscilla. J Biol Chem 255: 1478-1482.
38. Jacob W, Webster DA, Kroneck PM (1992) NADH-dependent methemoglobin reductase from the obligate aerobe Vitreoscilla: improved method of purification and reexamination of prosthetic groups. Arch Biochem Biophys 292: 29-33.
39. Rinaldi AC, Bonamore A, Macone A, Boffi A, Bozzi A, Di Gulio A (2006) Interaction of Vitreoscilla hemoglobin with membrane lipids. Biochemistry 45: 4069-4076.
40. Isarankura-Na-Ayudhya C, Panpumthong P, Tangkosakul T, Boonpangrak S, Prachayasittikul V (2008) Shedding light on the role of Vitreoscilla hemoglobin on cellular catabolic regulation by proteomic analysis. Int J Biol Sci 4: 71-80. (Pubitemid 351872042)
41. Khosla C, Bailey JE (1989) Characterization of the oxygen-dependent promoter of the Vitreoscilla hemoglobin gene in Escherichia coli. J Bacteriol 171: 5995-6004. (Pubitemid 19266922)
42. Joshi M, Dikshit KL (1994) Oxygen dependent regulation of Vitreoscilla globin gene: evidence for positive regulation by FNR. Biochem Biophys Res Comm 202: 535-542.
43. Yang J, Webster DA, Stark BC (2005) ArcA works with Fnr as a positive regulator of Vitreoscilla (bacterial) hemoglobin gene expression in Escherichia coli. Microbiol Res 160: 405-415. (Pubitemid 41266937)
44. Webster DA (1975) The formation of hydrogen peroxide during the oxidation of reduced nicotinamide adenine dinucleotide by cytochrome o from Vitreoscilla. J Biol Chem 250: 4955-4958.
45. Orii Y, Webster DA (1977) Oxygenated cytochrome o {Vitreoscilla) formed by treating oxidized cytochrome with superoxide anion. Plant & Cell Physiol 18: 521-526.
46. Chen R, Bailey JE (1994) Energetic effect of Vitreoscilla hemoglobin expression in Escherichia coli: an online 31P NMR and saturation transfer study. Biotechnol Prog 10: 360-364. (Pubitemid 2129363)
47. Kallio PT, Kim DJ, Tsai PS, Bailey JE (1994) Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. Eur J Biochem 219: 201-208. (Pubitemid 24053634)
48. Tsai PS, Hatzimanikatis V, Bailey JE (1996) Effect of Vitreoscilla hemoglobin dosage on microaerobic Escherichia coli carbon and energy metabolism. Biotechnol Bioeng 49: 139-150. (Pubitemid 26011767)
49. Tsai PS, Rao G, Bailey JE (1995) Improvement of Escherichia coli microaerobic oxygen metabolism by Vitreoscilla hemoglobin: new insights from NAD(P)H fluorescence and culture redox potential. Biotechnol Bioeng 47: 347-354.
50. Frey AD, Fiaux J, Szyperski T, Wuthrich K, Bailey JE, Kallio PT (2001) Dissection of central carbon metabolism of hemoglobin-expressing Escherichia coli by 13C nuclear magnetic resonance flux distribution analysis in microaerobic bioprocesses. Appl Env Microbiol 67: 680-687. (Pubitemid 32121356)
51. Arnaldos M, Kunkel SA, Wang J, Pagilla KR, Stark BC (2012) Vitreoscilla hemoglobin enhances ethanol production by Escherichia coli in a variety of growth media. Biomass Bioenergy 37: 1-8.
52. Khosla C, Curtis JE, DeModena J, Rinas U, Bailey JE (1990) Expression of intracellular hemoglobin improves protein synthesis in oxygen-limited Escherichia coli. Nature Biotechnol 8: 849-853.
53. Chen W, Hughes DE, Bailey JE (1994) Intracellular expression of Vitreoscilla hemoglobin alters the aerobic metabolism of Saccharomyces cerevisiae. Biotechnol Prog 10: 308-313. (Pubitemid 2099392)
54. Wei M-L, Webster DA, Stark BC (1998) Metabolic engineering of Serratia marcescens with the bacterial hemoglobin gene: alterations in fermentation pathways. Biotechnol Bioeng 59: 640-646. (Pubitemid 28350466)
55. Geckil H, Barak Z, Chipman DM, Erenler SO, Webster DA, Stark BC (2004) Enhanced production of acetoin and butanediol in recombinant Enterobacter aerogenes carrying Vitreoscilla hemoglobin gene. Bioprocess Biosystems Engin 26: 325-330. (Pubitemid 39517867)
56. Liu SC, Webster DA, Wei ML, Stark BC (1996) Genetic engineering to contain the Vitreoscilla hemoglobin gene enhances degradation of benzoic acid by Xanthomonas maltophilia. Biotechnol Bioengin 49: 101-105. (Pubitemid 26001496)
57. Patel SM, Stark BC, Hwang KW, Dikshit KL, Webster DA (2000) Cloning and expression of Vitreoscilla hemoglobin gene in Burkholderia sp. strain DNT for enhancement of 2,4-dinitrotoluene degradation. Biotechnol Prog 16: 26-30. (Pubitemid 30097646)
58. Chung JW, Webster DA, Pagilla KR, Stark BC (2001) Chromosomal integration of the Vitreoscilla hemoglobin gene in Burkholderia and Pseudomonas for the purpose of producing stable engineered strains with enhanced bioremediating ability. J Indust Microbiol Biotechnol 27: 27-33. (Pubitemid 32959928)
59. Nasr MA, Hwang KW, Akbas M, Webster DA, Stark BC (2001) Effects of culture conditions on enhancement of 2,4-dinitrotoluene degradation by Burkholderia engineered with the Vitreoscilla hemoglobin gene. Biotechnol Prog 17: 359-361. (Pubitemid 32663402)
60. Urgun-Demirtas M, Pagilla KR, Stark B, Webster D (2003) Biodegradation of 2-chlorobenzoate by recombinant Burkholderia cepacia expressing Vitreoscilla hemoglobin under variable levels of oxygen availability. Biodegradation 14: 357-365. (Pubitemid 37205343)
61. Urgun-Demirtas M, Pagilla KR, Stark B (2004) Enhanced kinetics of genetically engineered Burkholderia cepacia: the role of vgb in the hypoxic cometabolism of 2-CBA. Biotechnol Bioeng 87: 110-118. (Pubitemid 38878744)
62. Urgun-Demirtas M, Stark BC, Pagilla KR (2005) 2-Chlorobenzoate biodegradation by recombinant Burkholderia cepacia under hypoxic conditions in a membrane bioreactor. Water Environ Res 77: 511-518. (Pubitemid 41383347)
63. So J, Webster DA, Stark BC, Pagilla KR (2004) Enhancement of 2,4-dinitrotoluene biodegradation by Burkholderia sp. in sand bioreactors using bacterial hemoglobin technology. Biodegradation 15: 161-171. (Pubitemid 38981791)
64. Kahraman H, Geckil H (2005) Degradation of benzene, toluene, and xylene by Pseudomonas aeruginosa engineered with the Vitreoscilla hemoglobin gene. Engin Life Sciences 5: 363-368. (Pubitemid 41358520)
65. Urgun-Demirtas M, Stark B, Pagilla K (2006) Use of genetically engineered microorganisms (GEMs) for the bioremediation of contaminants. Crit Rev Biotechnol 26: 145-164. (Pubitemid 44567664)
66. Stark BC, Urgun-Demirtas M, Pagilla KR (2008) Role of hemoglobin in improving biodegradation of aromatic contaminants under hypoxic conditions. J Mol Microbiol Biotechnol 15: 181-189.
67. Fish PA, Webster DA, Stark BC (2000) Vitreoscilla hemoglobin enhances the first step in 2,4-dinitrotoluene degradation in vitro and at low aeration in vivo. J Molec Catalysis B: Enzymatic 9: 75-82. (Pubitemid 30136054)
68. Dien BS, Nichols NN, O'Bryan PJ, Bothast RJ (2000) Development of new ethanologenic Escherichia coli strains for fermentation of lignocellulosic biomass. Appl Biochem Biotechnol 84-86: 181-196. (Pubitemid 30349459)
69. Sanny T, Arnaldos M, Kunkel SA, Pagilla KR, Stark BC (2010) Engineering of ethanolic E. coli with the Vitreoscilla hemoglobin gene enhances ethanol production from both glucose and xylose. Appl Microbiol Biotechnol 88: 1103-1112.
70. Althertum F, Ingram LO (1989) Efficient ethanol production from glucose, lactose, and xylose by recombinant Escherichia coli, Appl Environ Microbiol 55: 1943-48.
71. Jansen NB, Flickinger MC, Tsao GT (1984) Production of 2,3-butanediol from D-xylose by Klebsiella oxytoca ATCC 8724. Biotechnol Bioeng 26: 362-69. (Pubitemid 14114643)
72. Okuda N, Ninomiya K, Takao M, Katakura Y, Shioya S (2007) Microaeration enhances productivity of ethanol from hydrolysate of waste house wood using ethanologenic Escherichia coli KO11. J Biosci Bioeng 103: 350-57. (Pubitemid 46720084)
73. Nieves IU, Geddes CC, Mullinnix MT, Hoffman RW, Tong Z, Castro E, Shanmugam KT, Ingram LO (2011) Injection of air into the headspace improves fermentation of phosphoric acid pretreated sugarcane bagasse by Escherichia coli MM 170. Bioresource Technol 102: 6959-65.