Recent advances in understanding the structure, function, and biotechnological usefulness of the hemoglobin from the bacterium Vitreoscilla

Biotechnology Letters

Volumn 33, Issue 9, 2011, Pages 1705-1714

  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

Bioremediation enhancement; Enhancement of bioproduct production; Oxygen binding and delivery; Oxygen sensing; Vitreoscilla hemoglobin

Indexed keywords

BIOCHEMICAL FUNCTIONS; BIOTECHNOLOGICAL APPLICATIONS; HARMFUL COMPOUNDS; LIGAND BINDING PROPERTIES; OXYGEN BINDING AND DELIVERY; OXYGEN SENSING; POSITIVE EFFECTS; VITREOSCILLA; VITREOSCILLA HEMOGLOBIN;

BACTERIA; BINDING ENERGY; BIOREMEDIATION; BIOTECHNOLOGY; CLONING; GENE EXPRESSION; OXYGEN;

HEMOGLOBIN;

BACTERIAL PROTEIN; BIOLOGICAL PRODUCT; HEMOGLOBIN PROTEIN, VITREOSCILLA; RECOMBINANT PROTEIN; TRUNCATED HEMOGLOBIN;

BIOTECHNOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR CLONING; REVIEW; VITREOSCILLA;

BACTERIAL PROTEINS; BIOLOGICAL AGENTS; BIOTECHNOLOGY; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; RECOMBINANT PROTEINS; TRUNCATED HEMOGLOBINS; VITREOSCILLA;

BACTERIA (MICROORGANISMS); VITREOSCILLA;

EID: 80051474719     PISSN: 01415492     EISSN: 15736776     Source Type: Journal    
DOI: 10.1007/s10529-011-0621-9     Document Type: Review

References (77)

1. Anand A, Duk BT, Singh S, Akbas MY, Webster DA, Stark BC, Dikshit KL (2010) Redox mediated interactions of VHb (Vitreoscilla hemoglobin) with OxyR: novel regulation of VHb biosynthesis under oxidative stress. Biochem J 426: 271-280.
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. Boerman SJ, Webster DA (1982) Control of heme content in Vitreoscilla by oxygen. J Gen Appl Microbiol 28: 35-43.
4. Cao MX, Huang JQ, Wei ZM, Yao QH, Wan CZ, Lu JA (2004) Engineering higher yield and herbicide resistance in rice by Agrobacterium-mediated multiple gene transformation. Crop Sci 44: 2206-2213.
5. Chen H, Chu J, Zhang S, Zhuang Y, Qian J, Wang Y, Hu X (2007) Intracellular expression of Vitreoscilla hemoglobin improves S-adenosylmethionine production in a recombinant Pichia pastoris. Appl Microbiol Biotechnol 74: 1205-1212.
6. Chien LJ, Lee CK (2007) Enhanced hyaluronic acid production in Bacillus subtilis by coexpressing bacterial hemoglobin. Biotechnol Prog 23: 1017-1022.
7. Chien LJ, Chen HT, Yang PF, Lee CK (2006) Enhancement of cellulose pellicle production by constitutively expressing Vitreoscilla hemoglobin in Acetobacter xylinum. Biotechnol Prog 22: 1598-1603.
8. DeMaio RA, Webster DA, Chance B (1983) Spectral evidence for the existence of a second cytochrome o in whole cells of Vitreoscilla. J Biol Chem 258: 13768-13771.
9. Dikshit KL, Webster DA (1988) Cloning, characterization and expression of the bacterial globin gene from Vitreoscilla in Escherichia coli. Gene 70: 377-386.
10. 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.
11. 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.
12. 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.
13. Dogan I, Pagilla KR, Webster DA, Stark BC (2006) Expression of Vitreoscilla hemoglobin in Gordonia amarae enhances biosurfactant production. J Ind Microbiol Biotechnol 33: 693-700.
14. 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.
15. Feng L, Chen S, Sun M, Yu Z (2007) Expression of Vitreoscilla hemoglobin in Bacillus thuringiensis improves the cell density and crystal proteins yield. Appl Microbiol Biotechnol 74: 390-397.
16. Frey AD, Kallio PT (2003) Bacterial hemoglobins and flavohemoglobins: versatile proteins and their impact on microbiology and biotechnology. FEMS Microbiol Rev 27: 525-545.
17. Geckil H, Gencer S, Kahraman H, Erenler SO (2003) Genetic engineering of Enterobacter aerogenes with Vitreoscilla hemoglobin gene: cell growth, survival, and antioxidant enzyme status under oxidative stress. Res in Microbiol 154: 425-431.
18. Geckil H, Gencer S, Ates B, Ozer U, Uckun M, Yilmaz I (2006) Effect of Vitreoscilla hemoglobin on production of a chemotherapeutic enzyme, L-asparaginase, by Pseudomonas aeruginosa. Biotechnol J 1: 203-208.
19. Holmberg N, Lilius G, Bailey JE, Bülow L (1997) Transgenic tobacco expressing Vitreoscilla hemoglobin exhibits enhanced growth and altered metabolite production. Nat Biotechnol 15: 244-247.
20. Horng YT, Chang KC, Chien CC, Wei YH, Sun YM, Soo PC (2010) Enhanced polyhydroxybutyrate (PHB) production via the coexpressed phaCAB and vgb genes controlled by arabinose P-BAD promoter in Escherichia coli. Lett Appl Microbiol 50: 158-167.
21. 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 3: 71-80.
22. Jokipii S, Häggman H, Brader G, Kallio PT, Niemi K (2008) Endogenous PttHb1 and PttTrHb, and heterologous Vitreoscilla vhb haemoglobin gene expression in hybrid aspen roots with ectomycorrhizal interaction. J Exp Botany 59: 2449-2459.
23. Kahraman H, Geckil H (2005) Degradation of benzene, toluene and xylene by Pseudomonasaeruginosa engineered with the Vitreoscilla hemoglobin gene. Eng Life Sci 5: 363-368.
24. Kallio PT, Bollinger CJ, Koskenkorva T, Frey AD (2008) Assessment of biotechnologically relevant characteristics of heterologous hemoglobins in E. coli. Methods Enzymol 436: 255-272.
25. Kaur R, Pathania R, Sharma V, Mande SC, Dikshit KL (2002) Chimeric Vitreoscilla hemoglobin (VHb) carrying a flavoreductase domain relieves nitrosative stress in Escherichia coli: new insight into the functional role of VHb. Appl Environ Microbiol 68: 152-160.
26. 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 Tyr126(H12). FEBS Lett 582: 2494-3500.
27. Khleifat KM, Abboud MM, Al-Mustafa AH (2006) Effect of Vitreoscilla hemoglobin gene (vgb) and metabolic inhibitors on cadmium uptake by the heterologous host Enterobacter aerogenes. Process Biochem 41: 930-934.
28. Khosla C, Bailey JE (1988) Heterologous expression of a bacterial hemoglobin improves the growth properties of recombinant Escherichia coli. Nature 331: 633-635.
29. 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.
30. Kim D, Hwang DS, Kang DG, Kim JY, Cha HJ (2008) Enhancement of mussel adhesive protein production in Escherichia coli by co-expression of bacterial hemoglobin. Biotechnol Prog 24: 663-666.
31. Krooneman J, Wieringa EBA, Moore ERB, Gerritse J, Prins RA, Gottschal JC (1996) Isolation of Alcaligenes sp. strain L6 at low oxygen concentrations and degradation of 3-chlorobenzoate via a pathway not involving (chloro) catechols. Appl Environ Microbiol 62: 2427-2434.
32. Kurt AG, Aytan E, Ozer U, Ates B, Geckil H (2009) Production of L-DOPA and dopamine in recombinant bacteria bearing the Vitreoscilla hemoglobin gene. Biotechnol J 4: 1077-1088.
33. Kvist M, Ryabova ES, Nordlander E, Bulow L (2007) An investigation of the peroxidase activity of Vitreoscilla hemoglobin. J Biol Inorg Chem 12: 324-334.
34. Lee SY, Stark BC, Webster DA (2004) Structure-function of the Vitreoscilla hemoglobin D-region. Biochem Biophys Res Comm 316: 1101-1106.
35. Lee MJ, Duong CTF, Han K, Kim ES (2009) Combination strategy to increase cyclosporin A productivity by Tolypocladium niveum using random mutagenesis and protoplast transformation. J Microbiol Biotechnol 19: 869-872.
36. Li X, Peng RH, Fan HQ, Xiaong AS, Yao QH, Cheng ZM, Li Y (2005) Vitreoscilla hemoglobin overexpression increases submergence tolerance in cabbage. Plant Cell Rep 23: 710-715.
37. Li B, Li S, Zhou Y, Zhao X, Zhu B (2006) Cloning and expression of Vitreoscilla hemoglobin gene (vgb) in Penicillium chrysogenum. Zhongguo Kangshengsu Zazhi 31: 400-402.
38. Li H, Yu Z, Xiong X, Li Y, Wang H, Li X (2009) Expression of Vitreoscilla hemoglobin gene in Pseudomonas delafieldii R-8 and its application to diesel desulfurization. Wei Sheng Wu Xue Bao 49: 1026-1032.
39. Li M, Wu J, Lin J, Wei D (2010) Expression of Vitreoscilla hemoglobin enhances cell growth and dihydroxyacetone production in Gluconobacter oxydans. Curr Microbiol 61: 370-375.
40. 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.
41. Liu Q, Zhang J, Wei XX, Ouyang SP, Wu Q, Chen GQ (2008) Microbial production of l-glutamate and l-glutamine by recombinant Corynebacterium glutamicum harboring Vitreoscilla hemoglobin gene vgb. Appl Microbiol Biotechnol 77: 1297-1304.
42. Liu Y, Gong G, Xie L, Yuan N, Zhu C, Zhu B, Hu Y (2010) Improvement of cephalosporin C production by recombinant DNA integration in Acremonium chrysogenum. Mol Biotechnol 44: 101-109.
43. Lu XY, Wu Q, Zhang WJ, Zhang G, Chen GQ (2004) Molecular cloning of polyhydroxyalkanoate synthesis operon from Aeromonas hydrophila and its expression in Escherichia coli. Biotechnol Prog 20: 1332-1336.
44. Nilsson M, Kallio PT, Bailey JE, Bülow L, Wahlund KG (1999) Expression of Vitreoscilla hemoglobin in Escherichia coli enhances ribosome and tRNA levels: a flow field-flow fractionation study. Biotechnol Prog 15: 158-163.
45. Ouyang SP, Liu Q, Sun SY, Chen JC, Chen GQ (2007) Genetic engineering of Pseudomonas putida KY2442 for biotransformation of aromatic compounds to chiral cis-diols. J Biotechnol 132: 246-250.
46. 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.
47. Priscila G, Fernandez FJ, Absalon AE, Suarez MR, Sainoz M, Barrios-Gonzalez J, Mejia A (2008) Expression of the bacterial hemoglobin gene from Vitreoscilla stercoraria increases rifamycin B production in Amycolatopsis mediterranei. J Biosci Bioeng 106: 493-497.
48. 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.
49. Roos V, Andersson CI, Bülow L (2004) Gene expression profiling of Escherichia coli expressing double Vitreoscilla haemoglobin. J Biotechnol 114: 107-120.
50. 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.
51. 2 tension maximizes bacterial pellicle production. J Biotechnol 132: 38-43.
52. Shen XW, Yang Y, Jian J, Wu Q, Chen GQ (2009) Production and characterization of homopolymer poly(3-hydroxyvalerate) (PHV) accumulated by wild type and recombinant Aeromonas hydrophila strain 4AK4. Bioresour Technol 100: 4296-4299.
53. 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.
54. Su Y, Li X, Liu Q, Hou Z, Zhu X, Guo X, Ling P (2010) Improved poly-gamma-glutamic acid production by chromosomal integration of the Vitreoscilla hemoglobin gene (vgb) in Bacillus subtilis. Bioresour Technol 101: 4733-4736.
55. Suthar DH, Chattoo BB (2006) Expression of Vitreoscilla hemoglobin enhances growth and levels of alpha-amylase in Schwanniomyces occidentalis. Appl Microbiol Biotechnol 72: 94-102.
56. Tao L, Sedkova N, Yao H, Ye RW, Sharpe PL, Cheng Q (2007) Expression of bacterial hemoglobin genes to improve astaxanthin production in a methanotrophic bacterium Methylomonas species. Appl Microbiol Biotechnol 74: 625-633.
57. 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.
58. 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.
59. 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.
60. 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.
61. Urgun-Demirtas M, Pagilla KR, Stark BC (2006) Comparison of 2-chlorobenzoic acid biodegradation in a membrane bioreactor by B. cepacia and B. cepacia bearing the bacterial hemoglobin gene. Water Res 40: 3123-3130.
62. 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.
63. Vinogradov SN, Hoogewijs D, Bailey X, Arredondo-Peter R, Gough J, Dewilde S, Moens L, Vanfleteren JR (2006) A phylogenomic profile of globins. BMC Evol Biol 6: 31.
64. Wakabayashi S, Matsubara H, Webster DA (1986) Primary sequence of a dimeric bacterial hemoglobin from Vitreoscilla. Nature 322: 481-483.
65. Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2009) Functional expression of Vitreoscilla hemoglobin (VHb) in Arabadopsis relieves submergence, nitrosative, photooxidative stress and enhances antioxidants metabolism. Plant Sci 176: 66-77.
66. 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.
67. Webster DA (1987) Structure and function of bacterial hemoglobin and related proteins. In: Eichorn GC, Marzilli LG (eds) Advances in inorganic biochemistry, vol 7. Elsevier, New York, pp 245-265.
68. Webster DA, Hackett DP (1966) The purification and properties of cytochrome o from Vitreoscilla. J Biol Chem 241: 3308-3315.
69. Wilhelmson A, Hakkinen ST, Kallio PT, Oksman-Caldentey KM, Nuutila AM (2006) Heterologous expression of Vitreoscilla hemoglobin (VHb) and cultivation conditions affect the alkaloid profile of Hyoscyamus muticus hairy roots. Biotechnol Prog 22: 350-358.
70. Wu Y, Wang H, Sun Y, Wu Q, Feng L, Zhang Z, Yang Q, Yang G (2007) Expression of Vitreoscilla hemoglobin gene in Saccharopolyspora erythraea and its effect on erythromycin production. Zhongguo Kangshengsu Zahzi 32: 599-601.
71. Xiong X, Xing J, Li X, Bai X, Li W, Li Y, Liu H (2007) Enhancement of biodesulfurization in two-liquid systems by heterogeneous expression of Vitreoscilla hemoglobin. Appl Environ Microbiol 73: 2394-2397.
72. 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.
73. Yang YC, Hong CF, Chao YP (2009) Effect of transformation of vhb gene on bacterial cellulose production of Gluconacetobacter xylinus. Bull Taiching Dist Agric Improv Stn 102: 1-14.
74. Yu H, Ma X, Luo H, Wen C, Shen Z (2008) Fusion expression of D-amino acid oxidase from Trignoposis variabilis with maltose binding protein and Vitreoscilla hemoglobin. Sheng Wu Gong Cheng Xue Bao 24: 1004-1009.
75. Zelasco S, Reggi S, Calligari P, Balestrazzi A, Bongiorni C, Quattrini E, Delia G, Bisoffi S, Fogher C, Confalonieri M (2006) Expression of the Vitresocilla hemoglobin (VHb)-encoding gene in transgenic white poplar: plant growth and biomass production, biochemical characterization and cell survival under submergence, oxidative and nitrosative stress conditions. Mol Breed 17: 201-216.
76. 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.
77. Zhu H, Sun S, Zhang S (2010) Enhanced production of total flavones and exopolysaccharides via Vitreoscilla hemoglobin biosynthesis in Phellinus igniarius. Bioresour Technol (in press).