Bacterial hemoglobins and flavohemoglobins: Versatile proteins and their impact on microbiology and biotechnology

FEMS Microbiology Reviews

Volumn 27, Issue 4, 2003, Pages 525-545

  Frey, Alexander D ^a,b   Kallio, Pauli T ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Biotechnological application; Microaerobic growth; Nitric oxide detoxification; Nitrosative stress; Pathogenic bacteria; Protein engineering

Indexed keywords

BACTERIAL PROTEIN; FLAVOHEMOGLOBIN; HEMOGLOBIN; NITRIC OXIDE; NITROGEN; UNCLASSIFIED DRUG; VITREOSCILLA HEMOGLOBIN;

AEROBIC METABOLISM; AQUIFEX AEOLICUS; AZOTOBACTER VINELANDII; BACILLUS ANTHRACIS; BACILLUS HALODURANS; BACILLUS SUBTILIS; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOTECHNOLOGY; BURKHOLDERIA; CAMPYLOBACTER JEJUNI; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELLULAR DISTRIBUTION; CHEMICAL ANALYSIS; CHEMICAL REACTION; CLOSTRIDIUM PERFRINGENS; CORYNEBACTERIUM GLUTAMICUM; DEINOCOCCUS RADIODURANS; DETOXIFICATION; ENERGY YIELD; ERWINIA; ESCHERICHIA COLI; HETEROLOGOUS EXPRESSION; MICROBIOLOGY; NITROSATION; NONHUMAN; NOSTOC; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRODUCTIVITY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; RALSTONIA METALLIDURANS; RALSTONIA SOLANACEARUM; REVIEW; RHODOPSEUDOMONAS PALUSTRIS; SALMONELLA ENTERICA; SEQUENCE HOMOLOGY; SHIGELLA FLEXNERI; SINORHIZOBIUM MELILOTI; STAPHYLOCOCCUS AUREUS; STREPTOMYCES COELICOLOR; VIBRIO CHOLERAE; VIBRIO PARAHAEMOLYTICUS; VITREOSCILLA; WAUTERSIA EUTROPHA; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); VITREOSCILLA; VITREOSCILLA SP.;

EID: 0141783647     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-6445(03)00056-1     Document Type: Review

References (167)

1. Perutz M.F. Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annu. Rev. Biochem. 48:1979;327-386.
2. Perutz M.F. Structure and function of hemoglobin. Harvey Lect. 63:1969;213-261.
3. Burmester T., Weich B., Reinhardt S., Hankein T. A vertebrate globin expressed in the brain. Nature. 407:2000;520-523.
4. Burmester T., Ebner B., Weich B., Hankeln T. Cytoglobin: a novel globin type ubiquitously expressed in vertebrate tissues. Mol. Biol. Evol. 19:2002;416-421.
5. Trent J.T. III, Hargrove M.S. A ubiquitously expressed human hexacoordinate hemoglobin. J. Biol. Chem. 277:2002;239-248.
6. Sun Y., Jin K., Mao X.O., Zhu Y., Greenberg D.A. Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury. Proc. Natl. Acad. Sci. USA. 98:2001;15306-15311.
7. Weber R.E., Vinogradov S.N. Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol. Rev. 81:2001;569-628.
8. Wakabayashi S., Matsubara H., Webster D.A. Primary sequence of a dimeric bacterial haemoglobin from Vitreoscilla. Nature. 322:1986;481-483.
9. Taylor E.R., Nie X.Z., Macgregor A.W., Hill R.D. A cereal hemoglobin gene is expressed in seed and root tissues under anaerobic conditions. Plant Mol. Biol. 24:1994;853-862.
10. Couture M., Chamberland H., St-Pierre B., Lafontaine J., Guertin M. Nuclear genes encoding chloroplast hemoglobins in the unicellular green alga Chlamydomonas eugametos. Mol. Gen. Genet. 243:1994;185-197.
11. Andersson C.R., Jensen E.O., Lewellyn D.J.L.L., Dennis E.S., Peacock W.J. A new hemoglobin gene from soybean: a role for hemoglobin in all plants. Proc. Natl. Acad. Sci. USA. 93:1996;5682-5687.
12. 2-binding kinetics of a recombinant protein synthesized in Escherichia coli. Plant Physiol. 115:1997;1259-1266.
13. Probst I., Wolf G., Schlegel H.G. An oxygen-binding flavohemoprotein from Alcaligenes eutrophus. Biochim. Biophys. Acta. 576:1979;471-478.
14. Zhu H., Riggs A.F. Yeast flavohemoglobin is an ancient protein related to globins and a reductase family. Proc. Natl. Acad. Sci. USA. 89:1992;5015-5019.
15. Takaya N., Suzuki S., Matsuo M., Shoun H. Purification and characterization of a flavohemoglobin from the denitrifying fungus Fusarium oxysporum. FEBS Lett. 414:1997;545-548.
16. Iijima M., Shimizu H., Tanaka Y., Urushihara H. Identification and characterization of two flavohemoglobin genes in Dictyostelium discoideum. Cell Struct. Funct. 25:2000;47-55.
17. Iwaasa H., Takagi T., Shikama K. Protozoan myoglobin from Paramecium caudatum. Its unusual amino acid sequence. J. Mol. Biol. 208:1989;355-358.
18. Potts M., Angeloni S.V., Ebel R.E., Bassam D. Myoglobin in a cyanobacterium. Science. 256:1992;1690-1692.
19. 2 diffusion to the heme. EMBO J. 20:2001;3902-3909.
20. Watts R.A., Hunt P.W., Hvitved A.N., Hargrove M.S., Peacock W.J., Dennis E.S. A hemoglobin from plants homologous to truncated hemoglobins of microorganisms. Proc. Natl. Acad. Sci. USA. 98:2001;10119-10124.
21. Wittenberg J.B., Bolognesi M., Wittenberg B.A., Guertin M. Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes and plants. J. Biol. Chem. 277:2002;871-874.
22. Takagi T. Hemoglobins from single-celled organisms. Curr. Opin. Struct. Biol. 3:1993;413-418.
23. Webster D.A., Hackett D.P. The purification and properties of cytochrome o from Vitreoscilla. J. Biol. Chem. 241:1966;3308-3315.
24. Webster D.A., Liu C.Y. Reduced nicotinamide adenine dinucleotide cytochrome o reductase associated with cytochrome o purified from Vitreoscilla. Evidence for an intermediate oxygenated form of cytochrome o. J. Biol. Chem. 249:1974;4257-4260.
25. Orii Y., Webster D.A. Photodissociation of oxygenated cytochrome o(s) (Vitreoscilla) and kinetic studies of reassociation. J. Biol. Chem. 261:1986;3544-3547.
26. Dikshit K.L., Webster D.A. Cloning, characterization and expression of the bacterial globin gene from Vitreoscilla in Escherichia coli. Gene. 70:1988;377-386.
27. Khosla C., Bailey J.E. The Vitreoscilla hemoglobin gene: molecular cloning, nucleotide sequence and genetic expression in Escherichia coli. Mol. Gen. Genet. 214:1988;158-161.
28. Gonzales-Prevatt V., Webster D.A. Purification and properties of NADH-cytochrome o reductase from Vitreoscilla. J. Biol. Chem. 255:1980;1478-1482.
29. Webster D.A. Structure and function of bacterial hemoglobin and related proteins. Adv. Inorg. Biochem. 7:1988;245-265.
30. Bollinger C.J.T., Bailey J.E., Kallio P.T. Novel hemoglobins to enhance microaerobic growth and substrate utilization in Escherichia coli. Biotechnol. Prog. 17:2001;798-808.
31. Frey A.D., Farrés J., Bollinger C.J.T., Kallio P.T. Bacterial hemoglobins and flavohemoglobins for alleviation of nitrosative stress in Escherichia coli. Appl. Environ. Microbiol. 68:2002;4835-4840.
32. Weihs V., Schmidt K., Schneider B., Friedrich B. The formation of an oxygen-binding flavohemoprotein in Alcaligenes eutrophus is plasmid-determined. Arch. Microbiol. 151:1989;546-550.
33. Cramm R., Siddiqui R.A., Friedrich B. Primary sequence and evidence for a physiological function of the flavohemoprotein of Alcaligenes eutrophus. J. Biol. Chem. 269:1994;7349-7354.
34. Vasudevan S.G., Armarego W.L.F., Shaw D.C., Lilley P.E., Dixon N.E., Poole R.K. Isolation and nucleotide-sequence of the hmp gene that encodes a hemoglobin-like protein in Escherichia coli K-12. Mol. Gen. Genet. 226:1991;49-58.
35. Crawford M.J., Goldberg D.E. Role for the Salmonella flavohemoglobin in protection from nitric oxide. J. Biol. Chem. 273:1998;12543-12547.
36. Crawford M.J., Goldberg D.E. Regulation of the Salmonella typhimurium flavohemoglobin gene. A new pathway for bacterial gene expression in response to nitric oxide. J. Biol. Chem. 273:1998;34028-34032.
37. LaCelle M., Kumano M., Kurita K., Yamane K., Zuber P., Nakano M.M. Oxygen-controlled regulation of the flavohemoglobin gene in Bacillus subtilis. J. Bacteriol. 178:1996;3803-3808.
38. Favey S., Labesse G., Vouille V., Boccara M. Flavohaemoglobin HmpX: a new pathogenicity determinant in Erwinia chrysanthemistrain 3937. Microbiology. 141:1995;863-871.
39. Hu Y.M., Butcher P.D., Mangan J.A., Rajandream M.A., Coates A.R.M. Regulation of hmp gene transcription in Mycobacterium tuberculosis: Effects of oxygen limitation and nitrosative and oxidative stress. J. Bacteriol. 181:1999;3486-3493.
40. Khosla C., Bailey J.E. Evidence for partial export of Vitreoscilla hemoglobin into the periplasmic space in Escherichia coli. Implications for protein function. J. Mol. Biol. 210:1989;79-89.
41. Inouye S., Duffaud G., Inouye M. Structural requirement at the cleavage site for efficient processing of the lipoprotein secretory precursor of Escherichia coli. J. Biol. Chem. 261:1986;10970-10975.
42. Ramandeep H.K.W., Raje M., Kim K.J., Stark B.C., Dikshit K.L., Webster D.A. Vitreoscilla hemoglobin. Intracellular localization and binding to membranes. J. Biol. Chem. 276:2001;24781-24789.
43. Vasudevan S.G., Tang P., Dixon N.E., Poole R.K. Distribution of the flavohaemoglobin, HMP, between periplasm and cytoplasm in Escherichia coli. FEMS Microbiol. Lett. 125:1995;219-224.
44. Ermler U., Siddiqui R.A., Cramm R., Schröder D., Friedrich B. Crystallization and preliminary X-ray diffraction studies of a bacterial flavohemoglobin protein. Proteins. 21:1995;351-353.
45. Ermler U., Siddiqui R.A., Cramm R., Friedrich B. Crystal structure of the flavohemoglobin from Alcaligenes eutrophus at 1.75 Å resolution. EMBO J. 14:1995;6067-6077.
46. Tarricone C., Calogero S., Galizzi A., Coda A., Ascenzi P., Bolognesi M. Expression, purification, crystallization and preliminary X-ray diffraction analysis of the homodimeric bacterial hemoglobin from Vitreoscilla stercoraria. Proteins. 27:1997;154-156.
47. Tarricone C., Galizzi A., Coda A., Ascenzi P., Bolognesi M. Unusual structure of the oxygen-binding site in the dimeric bacterial hemoglobin from Vitreoscilla sp. Structure. 5:1997;497-507.
48. Ilari A., Bonamore A., Farina A., Johnson K.A., Boffi A. The X-ray structure of ferric Escherichia coli flavohemoglobin reveals an unexpected geometry of the distal heme pocket. J. Biol. Chem. 277:2002;23725-23732.
49. Bolognesi M., Bordo D., Rizzi M., Tarricone C., Ascenzi P. Nonvertebrate hemoglobins: structural bases for reactivity. Prog. Biophys. Mol. Biol. 68:1997;29-68.
50. Ollesch G., Kaunzinger A., Juchelka D., Schubert-Zsilavecz M., Ermler U. Phospholipid bound to the flavohemoprotein from Alcaligenes eutrophus. Eur. J. Biochem. 262:1999;396-405.
51. Goodin D.B., McRee D.E. The Asp-His-Fe triad of cytochrome c peroxidase controls the reduction potential, electronic structure and coupling of the tryptophan free radical to the heme. Biochemistry. 32:1993;3313-3324.
52. Mukai M., Mills C.E., Poole R.K., Yeh S.R. Flavohemoglobin, a globin with a peroxidase-like catalytic site. J. Biol. Chem. 276:2001;7272-7277.
53. Choc M.G., Webster D.A., Caughey W.S. Oxygenated intermediate and carbonyl species of cytochrome o (Vitreoscilla). Characterization by infrared spectroscopy. J. Biol. Chem. 257:1982;865-869.
54. Bonamore A., Chiancone E., Boffi A. The distal heme pocket of Escherichia coli flavohemoglobin probed by infrared spectroscopy. Biochim. Biophys. Acta. 1549:2001;174-178.
55. Bolognesi M., Boffi A., Coletta M., Mozzarelli A., Pesce A., Tarricone C., Ascenzi P. Anticooperative ligand-binding properties of recombinant ferric Vitreoscilla homodimeric hemoglobin: a thermodynamic, kinetic and X-ray crystallographic study. J. Mol. Biol. 291:1999;637-650.
56. Dikshit K.L., Orii Y., Navani N., Patel S., Huang H.Y., Stark B.C., Webster D.A. Site-directed mutagenesis of bacterial hemoglobin: The role of glutamine (E7) in oxygen-binding in the distal heme pocket. Arch. Biochem. Biophys. 349:1998;161-166.
57. Stevanin T.M., Ioannidis N., Mills C.E., Kim S.O., Hughes M.N., Poole R.K. Flavohemoglobin hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo′ or bd, from nitric oxide. J. Biol. Chem. 275:2000;35868-35875.
58. +-reductase: prototype for a structurally novel flavoenzyme family. Science. 251:1991;60-66.
59. Bowien B., Schlegel H.G. Physiology and biochemistry of aerobic hydrogen-oxidizing bacteria. Annu. Rev. Microbiol. 35:1981;405-452.
60. Tyree B., Webster D.A. Intermediates in the reaction of reduced cytochrome o (Vitreoscilla) with oxygen. J. Biol. Chem. 254:1979;176-179.
61. Webster D.A., Orii Y. Oxygenated cytochrome o. An active intermediate observed in whole cells of Vitreoscilla. J. Biol. Chem. 252:1977;1834-1836.
62. Orii Y., Ioannidis N., Poole R.K. The oxygenated flavohaemoglobin from Escherichia coli: evidence from photodissociation and rapid-scan studies for two kinetic and spectral forms. Biochem. Biophys. Res. Commun. 187:1992;94-100.
63. Ioannidis N., Cooper C.E., Poole R.K. Spectroscopic studies on an oxygen-binding hemoglobin-like flavohaemoprotein from Escherichia coli. Biochem. J. 288:1992;649-655.
64. Giangiacomo L., Mattu M., Arcovito A., Bellenchi G., Bolognesi M., Ascenzi P., Boffi A. Monomer-dimer equilibrium and oxygen-binding properties of ferrous Vitreoscilla hemoglobin. Biochemistry. 40:2001;9311-9316.
65. Poole R.K., Rogers N.J., D'mello R.A.M., Hughes M.N., Orii Y. Escherichia coli flavohaemoglobin (Hmp) reduces cytochrome c and Fe(III)-hydroxamate K by electron transfer from NADH via FAD: Sensitivity of oxidoreductase activity to haem-bound dioxygen. Microbiology. 143:1997;1557-1565.
66. Membrillo-Hernández J., Ioannidis N., Poole R.K. The flavohaemoglobin (HMP) of Escherichia coli generates superoxide in vitro and causes oxidative stress in vivo. FEBS Lett. 382:1996;141-144.
67. Mills C.E., Sedelnikova S., Soballe B., Hughes M.N., Poole R.K. Escherichia coli flavohaemoglobin (Hmp) with equistoichiometric FAD and haem contents has a low affinity for dioxygen in the absence or presence of nitric oxide. Biochem. J. 353:2001;207-213.
68. Poole R.K., Ioannidis N., Orii Y. Reactions of the Escherichia coli flavohaemoglobin (Hmp) with NADH and near-micromolar oxygen: Oxygen affinity of NADH oxidase activity. Microbiology. 142:1996;1141-1148.
69. + reductases. FEBS Lett. 302:1992;247-252.
70. Eschenbrenner M., Coves J., Fontecave M. Ferric reductases in Escherichia coli: the contribution of the haemoglobin-like protein. Biochem. Biophys. Res. Commun. 198:1994;127-131.
71. Webster D.A. The formation of hydrogen peroxide during the oxidation of reduced nicotinamide adenine dinucleotide by cytochrome o from Vitreoscilla. J. Biol. Chem. 250:1975;4955-4958.
72. Gardner P.R., Costantino G., Salzman A.L. Constitutive and adaptive detoxification of nitric oxide in Escherichia coli - Role of nitric-oxide dioxygenase in the protection of aconitase. J. Biol. Chem. 273:1998;26528-26533.
73. Hausladen A., Gow A.J., Stamler J.S. Nitrosative stress: Metabolic pathway involving the flavohemoglobin. Proc. Natl. Acad. Sci. USA. 95:1998;14100-14105.
74. Gardner A.M., Martin L.A., Gardner P.R., Dou Y., Olson J.S. Steady-state and transient kinetics of Escherichia coli nitric oxide dioxygenase (flavohemoglobin) - The B10 tyrosine hydroxyl is essential for dioxygen binding and catalysis. J. Biol. Chem. 275:2000;12581-12589.
75. Gardner P.R., Gardner A.M., Martin L.A., Dou Y., Li T., Olson J.S., Zhu H., Riggs A.F. Nitric-oxide dioxygenase activity and function of flavohemoglobins. Sensitivity to nitric oxide and carbon monoxide inhibition. J. Biol. Chem. 275:2000;31581-31587.
76. Hausladen A., Gow A., Stamler J.S. Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen. Proc. Natl. Acad. Sci. USA. 98:2001;10108-10112.
77. Kaur R., Pathania R., Sharma V., Mande S.C., Dikshit K.L. 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. 68:2002;152-160.
78. Kim S.O., Orii Y., Lloyd D., Hughes M.N., Poole R.K. Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide. FEBS Lett. 445:1999;389-394.
79. Gardner A.M., Helmick R.A., Gardner P.R. Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem. 277:2002;8172-8177.
80. Hutchings M.I., Mandhana N., Spiro S. The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. J. Bacteriol. 184:2002;4640-4643.
81. Gomes C.M., Giuffre A., Forte E., Vicente J.B., Saraiva L.M., Brunori M., Teixeira M. A novel type of nitric-oxide reductase, Escherichia coli flavorubredoxin. J. Biol. Chem. 277:2002;25273-25276.
82. Khosla C., Bailey J.E. Characterization of the oxygen-dependent promoter of the Vitreoscilla hemoglobin gene in Escherichia coli. J. Bacteriol. 171:1989;5990-6004.
83. Dikshit K.L., Dikshit R.P., Webster D.A. Study of Vitreoscilla globin (vgb) gene expression and promoter activity in E. coli through transcriptional fusion. Nucleic Acids Res. 18:1990;4149-4155.
84. Magnolo S.K., Leenutaphong D.L., DeModena J.A., Curtis J.E., Bailey J.E., Galazzo J.L., Hughes D.E. Actinorhodin production by Streptomyces coelicolor and growth of Streptomyces lividans are improved by the expression of a bacterial hemoglobin. Bio-Technology. 9:1991;473-476.
85. Wei M.L., Webster D.A., Stark B.C. Metabolic engineering of Serratia marcescens with the bacterial hemoglobin gene: Alterations in fermentation pathways. Biotechnol. Bioeng. 59:1998;640-646.
86. Wei M.L., Webster D.A., Stark B.C. Genetic engineering of Serratia marcescens with bacterial hemoglobin gene: Effects on growth, oxygen utilization and cell size. Biotechnol. Bioeng. 57:1998;477-483.
87. Ramírez M., Valderrama B., Arrendondo-Peter R., Sobéron M., Mora J., Hernández G. Rhizobium etli genetically engineered for the heterologous expression of Vitreoscilla sp. hemoglobin: Effect on free-living and symbiosis. Mol. Plant Microbe Interact. 12:1999;1008-1015.
88. Patel S.M., Stark B.C., Hwang K.W., Dikshit K.L., Webster D.A. Cloning and expression of Vitreoscilla hemoglobin gene in Burkholderia sp. strain DNT for enhancement of 2,4-dinitrotoluene degradation. Biotechnol. Prog. 16:2000;26-30.
89. Khosla C., Bailey J.E. Heterologous expression of a bacterial haemoglobin improves the growth properties of recombinant Escherichia coli. Nature. 331:1988;633-635.
90. Poole R.K., Anjum M.F., Membrillo-Hernández J., Kim S.O., Hughes M.N., Stewart V. Nitric oxide, nitrite and Fnr regulation of hmp (flavohemoglobin) gene expression in Escherichia coli K-12. J. Bacteriol. 178:1996;5487-5492.
91. Khosla C., Curtis J.E., Bydalek P., Swartz J.R., Bailey J.E. Expression of recombinant proteins in Escherichia coli using an oxygen-responsive promoter. Bio-Technology. 8:1990;554-558.
92. Tsai P.S., Kallio P.T., Bailey J.E. FNR, a global transcriptional regulator of Escherichia coli, activates the Vitreoscilla hemoglobin (VHb) promoter and intracellular VHb expression increases cytochrome d promoter activity. Biotechnol. Prog. 11:1995;288-293.
93. Joshi M., Dikshit K.L. Oxygen-dependent regulation of Vitreoscilla globin gene: evidence for positive regulation by FNR. Biochem. Biophys. Res. Commun. 202:1994;535-542.
94. Spiro S. The FNR family of transcriptional regulators. Antonie van Leeuwenhoek. 66:1994;23-36.
95. Spiro S., Gaston K.L., Bell A.I., Roberts R.E., Busby S.J., Guest J.R. Interconversion of the DNA-binding specificities of two related transcription regulators, CRP and FNR. Mol. Microbiol. 4:1990;1831-1838.
96. Khosla C., Curtis J.E., DeModena J., Rinas U., Bailey J.E. Expression of intracellular hemoglobin improves protein synthesis in oxygen-limited Escherichia coli. Bio-Technology. 8:1990;849-853.
97. Tsai P.S., Nägeli M., Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin modifies microaerobic Escherichia coli metabolism through elevated concentration and specific activity of cytochrome o. Biotechnol. Bioeng. 49:1996;151-160.
98. Kallio P.T., Kim D.-J., Tsai P.S., Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin alters Escherichia coli energy metabolism under oxygen-limited conditions. Eur. J. Biochem. 219:1994;201-208.
99. Puustinen A., Wikström M. The heme groups of cytochrome o from Escherichia coli. Proc. Natl. Acad. Sci. USA. 88:1991;6122-6126.
100. Puustinen A., Finel M., Haltia T., Gennis R.B., Wikström M. Properties of the 2 terminal oxidases of Escherichia coli. Biochemistry. 30:1991;3936-3942.
101. Park K.W., Kim K.J., Howard A.J., Stark B.C., Webster D.A. Vitreoscilla hemoglobin binds to subunit I of cytochrome bo ubiquinol oxidases. J. Biol. Chem. 277:2002;33334-33337.
102. Chen W., Hughes D.E., Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin alters the aerobic metabolism of Saccharomyces cerevisiae. Biotechnol. Prog. 10:1994;308-313.
103. Dikshit R.P., Dikshit K.L., Liu Y.X., Webster D.A. The bacterial hemoglobin from Vitreoscilla can support the aerobic growth of Escherichia coli lacking terminal oxidases. Arch. Biochem. Biophys. 293:1992;241-245.
104. Tsai P.S., Rao G., Bailey J.E. Improvement of Escherichia coli microaerobic oxygen-metabolism by Vitreoscilla hemoglobin: new insights from NAD(P)H fluorescence and culture redox potential. Biotechnol. Bioeng. 47:1995;347-354.
105. Nilsson M., Kallio P.T., Bailey J.E., Bülow L., Wahlund K.G. Expression of Vitreoscilla hemoglobin in Escherichia coli enhances ribosome and tRNA levels: A flow field-flow fractionation study. Biotechnol. Prog. 15:1999;158-163.
106. Zalkin, H. and Nygaard, P. (1996) Biosynthesis of purine nucleotides. In: Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology, Vol 1. (Neidhardt, F.C., Curtiss III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S., Riley, M., Schaechter, M. and Umbarger, H.E., Eds.), pp. 561-579. ASM Press, Washington, DC.
107. 31P NMR and saturation-transfer study. Biotechnol. Prog. 10:1994;360-364.
108. Ryll T., Wagner R. Improved ion-pair high-performance liquid chromatographic method for the quantification of a wide variety of nucleotides and sugar-nucleotides in animal cells. J. Chromatogr. 570:1991;77-88.
109. Albe K.R., Butler M.H., Wright B.E. Cellular concentrations of enzymes and their substrates. J. Theor. Biol. 143:1990;163-195.
110. Stevanin T.M., Poole R.K., Demoncheaux E.A., Read R.C. Flavohemoglobin Hmp protects Salmonella enterica serovar Typhimurium from nitric oxide-related killing by human macrophages. Infect. Immun. 70:2002;4399-4405.
111. S), IHF and ppGpp in the expression of the hmp gene encoding the flavohemoglobin (Hmp) of Escherichia coli K-12. Mol. Gen. Genet. 254:1997;599-603.
112. Cruz-Ramos H., Crack J., Wu G., Hughes M.N., Scott C., Thomson A.J., Green J., Poole R.K. NO-sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO J. 21:2002;3235-3244.
113. Membrillo-Hernández J., Coopamah M.D., Channa A., Hughes M.N., Poole R.K. A novel mechanism for upregulation of the Escherichia coli K-12 hmp (flavohaemoglobin) gene by the 'NO releaser', S-nitrosoglutathione: nitrosation of homocysteine and modulation of MetR binding to the glyA-hmp intergenic region. Mol. Microbiol. 29:1998;1101-1112.
114. De Groote M.A., Testerman T., Xu Y., Stauffer G.V., Fang F.C. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science. 272:1996;414-416.
115. S. J. Bacteriol. 179:1997;3164-3170.
116. Anjum M.F., Ioannidis N., Poole R.K. Response of the NAD(P)H-oxidising flavohaemoglobin (Hmp) to prolonged oxidative stress and implications for its physiological role in Escherichia coli. FEMS Microbiol. Lett. 166:1998;219-223.
117. Membrillo-Hernández J., Coopamah M.D., Anjum M.F., Stevanin T.M., Kelly A., Hughes M.N., Poole R.K. The flavohemoglobin of Escherichia coli confers resistance to a nitrosating agent, a 'nitric oxide releaser', and paraquat and is essential for transcriptional responses to oxidative stress. J. Biol. Chem. 274:1999;748-754.
118. Poole R.K., Hughes M.N. New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36:2000;775-783.
119. D'Autréaux B., Touati D., Bersch B., Latour J.M., Michaud-Soret I. Direct inhibition by nitric oxide of the transcriptional ferric-uptake regulation protein via nitrosylation of the iron. Proc. Natl. Acad. Sci. USA. 99:2002;16619-16624.
120. Goretski J., Zafiriou O.C., Hollocher T.C. Steady-state nitric oxide concentrations during denitrification. J. Biol. Chem. 265:1990;11535-11538.
121. Clements L.D., Streips U.N., Miller B.S. Differential proteomic analysis of Bacillus subtilis nitrate respiration and fermentation in defined medium. Proteomics. 2:2002;1724-1734.
122. Nakano M.M., Zhu Y., Lacelle M., Zhang X., Hulett F.M. Interaction of ResD with regulatory regions of anaerobically induced genes in Bacillus subtilis. Mol. Microbiol. 37:2000;1198-1207.
123. Nakano M.M. Induction of ResDE-dependent gene expression in Bacillus subtilis in response to nitric oxide and nitrosative stress. J. Bacteriol. 184:2002;1783-1787.
124. Hu Y., Coates A.R. Increased levels of sigJ mRNA in late stationary-phase cultures of Mycobacterium tuberculosis detected by DNA array hybridisation. FEMS Microbiol. Lett. 202:2001;59-65.
125. Pathania R., Navani N.K., Rajamohan G., Dikshit K.L. Mycobacterium tuberculosis hemoglobin HbO associates with membranes and stimulates cellular respiration of recombinant Escherichia coli. J. Biol. Chem. 277:2002; 15293-15302.
126. Firoved A.M., Deretic V. Microarray analysis of global gene expression in mucoid Pseudomonas aeruginosa. J. Bacteriol. 185:2003;1071-1081.
127. Bolwell G.P. Role of active oxygen species and NO in plant defence responses. Curr. Opin. Plant Biol. 2:1999;287-294.
128. Gennis, R.B. and Stewart, V. (1996) Respiration. In: Escherichia coli and Salmonella. Cellular and Molecular Biology, Vol. 1 (Neidhardt, F.C., Curtiss III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S., Riley, M., Schaechter, M. and Umbarger, H.E., Eds.), pp. 217-261. ASM Press, Washington, DC.
129. Rice C.W., Hempfling W.P. Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli. J. Bacteriol. 134:1978;115-124.
130. Lin, E.C.C. (1996) Dissimilatory pathways for sugars, polyols and carboxylates. In: Escherichia coli and Salmonella. Cellular and Molecular Biology, Vol. 1 (Neidhardt, F.C., Curtiss III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S., Riley, M., Schaechter, M. and Umbarger, H.E., Eds.), pp. 307-342. ASM Press, Washington, DC.
131. Stewart V. Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol. Rev. 52:1988;190-232.
132. Clark D.P. The fermentation pathways of Escherichia coli. FEMS Microbiol. Rev. 63:1989;223-234.
133. Unden G., Bongaerts J. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim. Biophys. Acta. 1320:1997;217-234.
134. Konz J.O., King J., Cooney C.L. Effects of oxygen on recombinant protein expression. Biotechnol. Prog. 14:1998;393-409.
135. Bailey J.E. Toward a science of metabolic engineering. Science. 252:1991;1668-1675.
136. Brünker P., Minas W., Kallio P.T., Bailey J.E. Genetic engineering of an industrial strain of Saccharopolyspora erythraea for stable expression of the Vitreoscilla haemoglobin gene (vhb). Microbiology. 144:1998;2441-2448.
137. Minas W., Brünker P., Kallio P.T., Bailey J.E. Improved erythromycin production in a genetically engineered industrial strain of Saccharopolyspora erythraea. Biotechnol. Prog. 14:1998;561-566.
138. Suen W.C., Spain J.C. Cloning and characterization of Pseudomonas sp. strain DNT genes for 2,4-dinitrotoluene degradation. J. Bacteriol. 175:1993;1831-1837.
139. Nasr M.A., Hwang K.W., Akbas M., Webster D.A., Stark B.C. Effects of culture conditions on enhancement of 2,4-dinitrotoluene degradation by Burkholderia engineered with the Vitreoscilla hemoglobin gene. Biotechnol. Prog. 17:2001;359-361.
140. Doran P.M. Foreign protein production in plant tissue cultures. Curr. Opin. Biotechnol. 11:2000;199-204.
141. Huang S.Y., Chou C.J. Effect of gaseous composition on cell growth and secondary metabolite production in suspension culture of Stizolobium hassjoo cells. Bioprocess Eng. 23:2000;585-593.
142. Farrés J., Kallio P.T. Improved growth in tobacco suspension cultures expressing Vitreoscilla hemoglobin. Biotechnol. Prog. 18:2002;229-233.
143. Pendse G.J., Bailey J.E. Effect of Vitreoscilla hemoglobin expression on growth and specific tissue plasminogen activator productivity in recombinant Chinese hamster ovary cells. Biotechnol. Bioeng. 44:1994;1367-1370.
144. Bailey J.E., Sburlati A., Hatzimanikatis V., Lee K., Renner W.A., Tsai P.S. Inverse metabolic engineering: A strategy for directed genetic engineering of useful phenotypes. Biotechnol. Bioeng. 52:1996;109-121.
145. Andersson C.I.J., Holmberg N., Farrés J., Bailey J.E., Bülow L., Kallio P.T. Error-prone PCR of Vitreoscilla hemoglobin (VHb) to support the growth of microaerobic Escherichia coli. Biotechnol. Bioeng. 70:2000;446-455.
146. 13C nuclear magnetic resonance flux distribution analysis in microaerobic bioprocesses. Appl. Environ. Microbiol. 67:2001;680-687.
147. Roos V., Andersson C.I.J., Arfvidsson C., Wahlund K.G., Bülow L. Expression of double Vitreoscilla hemoglobin enhances growth and alters ribosome and tRNA levels in Escherichia coli. Biotechnol. Prog. 18:2002;652-656.
148. Frey A.D., Bailey J.E., Kallio P.T. Expression of Alcaligenes eutrophus flavohemoprotein and engineered Vitreoscilla hemoglobin-reductase fusion protein for improved hypoxic growth of Escherichia coli. Appl. Environ. Microbiol. 66:2000;98-104.
149. 13C-labeling of proteinogenic amino-acids. An efficient analytical tool to investigate intermediary metabolism. Eur. J. Biochem. 232:1995;433-448.
150. 13C NMR flux ratio analysis of Escherichia coli central carbon metabolism in microaerobic bioprocesses. J. Am. Chem. Soc. 121:1999;1407-1408.
151. Wittenberg J.B., Wittenberg B.A. Mechanisms of cytoplasmic hemoglobin and myoglobin function. Annu. Rev. Biophys. Biophys. Chem. 19:1990;217-241.
152. Kallio P.T., Tsai P.S., Bailey J.E. Expression of Vitreoscilla hemoglobin is superior to horse heart myoglobin or yeast flavohemoglobin expression for enhancing Escherichia coli growth in a microaerobic bioreactor. Biotechnol. Prog. 12:1996;751-757.
153. Gort A.S., Imlay J.A. Balance between endogenous superoxide stress and antioxidant defenses. J. Bacteriol. 180:1998;1402-1410.
154. Storz, G. and Zheng, M. (2000) Oxidative stress. In: Bacterial Stress Response (Storz, G. and Hengge-Aronis, R., Eds.), pp. 47-59. ASM Press, Washington, DC.
155. Bogdan C., Rollinghoff M., Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12:2000;64-76.
156. Nathan C., Shiloh M.U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA. 97:2000;8841-8848.
157. Ji X.B., Hollocher T.C. Reduction of nitrite to nitric oxide by enteric bacteria. Biochem. Biophys. Res. Commun. 157:1988;106-108.
158. Labesse G., Craescu C.T., Mispelter J., Chottard G., Marden M.C., Pin S., Forest E., Mornon J.P., Boccara M. Engineering, expression and biochemical characterization of the hemoglobin domain of a Erwinia chrysanthemi flavohemoprotein. Eur. J. Biochem. 253:1998;751-759.
159. DeModena J.A., Gutiérrez S., Velasco J., Fernández F.J., Fachini R.A., Galazzo J.L., Hughes D.E., Martín J.F. The production of cephalosporin C by Acremonium chrysogenum is improved by the intracellular expression of a bacterial hemoglobin. Bio-Technology. 11:1993;926-929.
160. Kallio P.T., Bailey J.E. Intracellular expression of Vitreoscilla hemoglobin (VHb) enhances total protein secretion and improves the production of α-amylase and neutral protease in Bacillus subtilis. Biotechnol. Prog. 12:1996;31-39.
161. Sander, F.C., Fachini, R.A., Hughes, D.E., Galazzo, J.L. and Bailey, J.E. (1994) Expression of Vitreoscilla hemoglobin in Corynebacterium glutamicum increases final concentration and yield of lysine. Proceedings of the 6th European Congress on Biotechnology, 1993 (Alberghina, L., Frontali, L. and Sensi, P., Eds.), pp. 607-610. Elsevier.
162. Khosravi M., Webster D.A., Stark B.C. Presence of the bacterial hemoglobin gene improves alpha-amylase production of a recombinant Escherichia coli strain. Plasmid. 24:1990;190-194.
163. Chung Y.J., Kim K.S., Jeon E.S., Park K.I., Park C.U. Effects of the Vitreoscilla hemoglobin gene on the expression of the ferritin gene in Escherichia coli. J. Biochem. Mol. Biol. 31:1998;503-507.
164. Holmberg N., Lilius G., Bailey J.E., Bülow L. Transgenic tobacco expressing Vitreoscilla hemoglobin exhibits enhanced growth and altered metabolite production. Nat. Biotechnol. 15:1997;244-247.
165. Geckil H., Stark B.C., Webster D.A. Cell growth and oxygen uptake of Escherichia coli and Pseudomonas aeruginosa are differently affected by the genetically engineered Vitreoscilla hemoglobin gene. J. Biotechnol. 85:2001;57-66.
166. Liu S.C., Webster D.A., Wei M.L., Stark B.C. Genetic engineering to contain the Vitreoscilla hemoglobin gene enhances degradation of benzoic acid by Xanthomonas maltophilia. Biotechnol. Bioeng. 49:1996;101-105.
167. Gardner P.R., Gardner A.M., Martin L.A., Salzman A.L. Nitric oxide dioxygenase: An enzymic function for flavohemoglobin. Proc. Natl. Acad. Sci. USA. 95:1998;10378-10383.