Metabolic deficiences revealed in the biotechnologically important model bacterium Escherichia coli BL21(DE3)

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Pinske, Constanze ^a   Bönn, Markus ^a   Krüger, Sara ^a   Lindenstrauß, Ute ^a   Sawers, R Gary ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FORMATE DEHYDROGENASE; METALLOPROTEIN; MOLYBDENUM; NICKEL IRON HYDROGENASE; NITRATE REDUCTASE; SELENIUM; ESCHERICHIA COLI PROTEIN; HYDROGENASE; NICKEL-IRON HYDROGENASE;

ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOTECHNOLOGICAL PROCEDURES; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; ESCHERICHIA COLI; ESCHERICHIA COLI BL 21; EXPERIMENTAL MODEL; FNR GENE; GENE STRUCTURE; ION TRANSPORT; METABOLIC DISORDER; NONHUMAN; NONSENSE MUTATION; PROTEIN SYNTHESIS; TRANSCRIPTION REGULATION; BIOTECHNOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI B;

BIOTECHNOLOGY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FORMATE DEHYDROGENASES; HYDROGENASE; MUTATION; NITRATE REDUCTASE;

EID: 79961064482     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022830     Document Type: Article

References (92)

1. Sawers R, Clark D, Böck A, (2004) Fermentative Pyruvate and Acetyl-Coenzyme A Metabolism. EcoSal- Escherichia coli and Salmonella: cellular and molecular biology.
2. Spiro S, Guest JR, (1991) Adaptive responses to oxygen limitation in Escherichia coli. Trends Biochem Sci 16: 310-314.
3. Schindelin H, Kisker C, Rajagopalan KV, (2001) Molybdopterin from molybdenum and tungsten enzymes. Adv Protein Chem 58: 47-94.
4. Berg BL, Stewart V, (1990) Structural genes for nitrate-inducible formate dehydrogenase in Escherichia coli K-12. Genetics 125: 691-702.
5. Forzi L, Sawers RG, (2007) Maturation of [NiFe]-hydrogenases in Escherichia coli. Biometals 20: 565-578.
6. Sawers R, Ballantine S, Boxer D, (1985) Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzyme. J Bacteriol 164: 1324-1331.
7. Böck A, King P, Blokesch M, Posewitz M, (2006) Maturation of hydrogenases. Adv Microb Physiol 51: 1-71.
8. Forzi L, Hellwig P, Thauer RK, Sawers RG, (2007) The CO and CN(-) ligands to the active site Fe in [NiFe]-hydrogenase of Escherichia coli have different metabolic origins. FEBS Lett 581: 3317-3321.
9. Lenz O, Zebger I, Hamann J, Hildebrandt P, Friedrich B, (2007) Carbamoylphosphate serves as the source of CN(-), but not of the intrinsic CO in the active site of the regulatory [NiFe]-hydrogenase from Ralstonia eutropha. FEBS Lett 581: 3322-3326.
10. Kaluarachchi H, Chan Chung KC, Zamble DB, (2010) Microbial nickel proteins. Nat Prod Rep 27: 681-694.
11. Wu L, Mandrand-Berthelot M, (1986) Genetic and physiological characterization of new Escherichia coli mutants impaired in hydrogenase activity. Biochimie 68: 167-179.
12. Wu L, Mandrand-Berthelot M, Waugh R, Edmonds C, Holt S, et al. (1989) Nickel deficiency gives rise to the defective hydrogenase phenotype of hydC and fnr mutants in Escherichia coli. Mol Microbiol 3: 1709-1718.
13. Sauter M, Böhm R, Böck A, (1992) Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol 6: 1523-1532.
14. Sawers G, (1994) The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie Van Leeuwenhoek 66: 57-88.
15. Abaibou H, Pommier J, Benoit S, Giordano G, Mandrand-Berthelot MA, (1995) Expression and characterization of the Escherichia coli fdo locus and a possible physiological role for aerobic formate dehydrogenase. J Bacteriol 177: 7141-7149.
16. Ruiz-Herrera J, DeMoss JA, (1969) Nitrate reductase complex of Escherichia coli K-12: participation of specific formate dehydrogenase and cytochrome b1 components in nitrate reduction. J Bacteriol 99: 720-729.
17. Böck A, Forchhammer K, Heider J, Leinfelder W, Sawers G, et al. (1991) Selenocysteine: the 21st amino acid. Mol Microbiol 5: 515-520.
18. Schwarz G, Mendel RR, Ribbe MW, (2009) Molybdenum cofactors, enzymes and pathways. Nature 460: 839-847.
19. Delbrück M, (1940) The growth of bacteriophage and lysis of the host. J Gen Physiol 23: 643-660.
20. Studier FW, Moffatt BA, (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
21. Studier FW, Daegelen P, Lenski RE, Maslov S, Kim JF, (2009) Understanding the differences between genome sequences of Escherichia coli B strains REL606 and BL21(DE3) and comparison of the E. coli B and K-12 genomes. J Mol Biol 394: 653-680.
22. Daegelen P, Studier FW, Lenski RE, Cure S, Kim JF, (2009) Tracing ancestors and relatives of Escherichia coli B, and the derivation of B strains REL606 and BL21(DE3). J Mol Biol 394: 634-643.
23. Akhtar MK, Jones PR, (2008) Deletion of iscR stimulates recombinant clostridial Fe-Fe hydrogenase activity and H2-accumulation in Escherichia coli BL21(DE3). Appl Microbiol Biotechnol 78: 853-862.
24. Jeong H, Barbe V, Lee CH, Vallenet D, Yu DS, et al. (2009) Genome sequences of Escherichia coli B strains REL606 and BL21(DE3). J Mol Biol 394: 644-652.
25. Schlensog V, Birkmann A, Böck A, (1989) Mutations in trans which affect the anaerobic expression of a formate dehydrogenase (fdhF) structural gene. Arch Microbiol 152: 83-89.
26. Birkmann A, Zinoni F, Sawers R, Böck A, (1987) Factors affecting transcriptional regulation of the formate-hydrogen-lyase pathway of Escherichia coli. Arch Microbiol 148: 44-51.
27. Ballantine S, Boxer D, (1985) Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J Bacteriol 163: 454-459.
28. Paschos A, Bauer A, Zimmermann A, Zehelein E, Böck A, (2002) HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturation. J Biol Chem 277: 49945-49951.
29. Pinske C, Sawers RG, (2010) The role of the ferric-uptake regulator Fur and iron homeostasis in controlling levels of the [NiFe]-hydrogenases in Escherichia coli. International Journal of Hydrogen Energy 35: 8938-8944.
30. Rossmann R, Sawers G, Böck A, (1991) Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol Microbiol 5: 2807-2814.
31. Navarro C, Wu LF, Mandrand-Berthelot MA, (1993) The nik operon of Escherichia coli encodes a periplasmic binding-protein-dependent transport system for nickel. Mol Microbiol 9: 1181-1191.
32. Hube M, Blokesch M, Böck A, (2002) Network of hydrogenase maturation in Escherichia coli: role of accessory proteins HypA and HybF. J Bacteriol 184: 3879-3885.
33. Waugh R, Boxer D, (1986) Pleiotropic hydrogenase mutants of Escherichia coli K12: growth in the presence of nickel can restore hydrogenase activity. Biochimie 68: 157-166.
34. Hausinger RP, (1987) Nickel utilization by microorganisms. Microbiol Rev 51: 22-42.
35. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, et al. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12: 291-299.
36. Paschos A, Glass R, Böck A, (2001) Carbamoylphosphate requirement for synthesis of the active center of [NiFe]-hydrogenases. FEBS Lett 488: 9-12.
37. Maier T, Binder U, Böck A, (1996) Analysis of the hydA locus of Escherichia coli: two genes (hydN and hypF) involved in formate and hydrogen metabolism. Arch Microbiol 165: 333-341.
38. Rangarajan E, Asinas A, Proteau A, Munger C, Baardsnes J, et al. (2008) Structure of [NiFe] hydrogenase maturation protein HypE from Escherichia coli and its interaction with HypF. J Bacteriol 190: 1447-1458.
39. Messenger S, Green J, (2003) FNR-mediated regulation of hyp expression in Escherichia coli. FEMS Microbiol Lett 228: 81-86.
40. Lutz S, Jacobi A, Schlensog V, Böhm R, Sawers G, et al. (1991) Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli. Mol Microbiol 5: 123-135.
41. Jamieson DJ, Higgins CF, (1984) Anaerobic and leucine-dependent expression of a peptide transport gene in Salmonella typhimurium. J Bacteriol 160: 131-136.
42. Sawers RG, (2005) Expression of fnr is constrained by an upstream IS5 insertion in certain Escherichia coli K-12 strains. J Bacteriol 187: 2609-2617.
43. Richard D, Sawers G, Sargent F, McWalter L, Boxer D, (1999) Transcriptional regulation in response to oxygen and nitrate of the operons encoding the [NiFe] hydrogenases 1 and 2 of Escherichia coli. Microbiology 145: 2903-2912.
44. Brøndsted L, Atlung T, (1994) Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli. J Bacteriol 176: 5423-5428.
45. Sawers G, Böck A, (1988) Anaerobic regulation of pyruvate formate-lyase from Escherichia coli K-12. J Bacteriol 170: 5330-5336.
46. Sawers G, Böck A, (1989) Novel transcriptional control of the pyruvate formate-lyase gene: upstream regulatory sequences and multiple promoters regulate anaerobic expression. J Bacteriol 171: 2485-2498.
47. Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD, (1997) Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science 275: 1305-1308.
48. Schlindwein C, Giordano G, Santini CL, Mandrand MA, (1990) Identification and expression of the Escherichia coli fdhD and fdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J Bacteriol 172: 6112-6121.
49. Hall DR, Gourley DG, Leonard GA, Duke EM, Anderson LA, et al. (1999) The high-resolution crystal structure of the molybdate-dependent transcriptional regulator (ModE) from Escherichia coli: a novel combination of domain folds. EMBO J 18: 1435-1446.
50. Rosentel JK, Healy F, Maupin-Furlow JA, Lee JH, Shanmugam KT, (1995) Molybdate and regulation of mod (molybdate transport), fdhF, and hyc (formate hydrogenlyase) operons in Escherichia coli. J Bacteriol 177: 4857-4864.
51. Anderson LA, McNairn E, Lubke T, Pau RN, Boxer DH, et al. (2000) ModE-dependent molybdate regulation of the molybdenum cofactor operon moa in Escherichia coli. J Bacteriol 182: 7035-7043.
52. Hasona A, Self WT, Ray RM, Shanmugam KT, (1998) Molybdate-dependent transcription of hyc and nar operons of Escherichia coli requires MoeA protein and ModE-molybdate. FEMS Microbiol Lett 169: 111-116.
53. McNicholas PM, Gunsalus RP, (2002) The molybdate-responsive Escherichia coli ModE transcriptional regulator coordinates periplasmic nitrate reductase (napFDAGHBC) operon expression with nitrate and molybdate availability. J Bacteriol 184: 3253-3259.
54. Zinoni F, Birkmann A, Leinfelder W, Böck A, (1987) Cotranslational insertion of selenocysteine into formate dehydrogenase from Escherichia coli directed by a UGA codon. Proc Natl Acad Sci U S A 84: 3156-3160.
55. Miroux B, Walker JE, (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260: 289-298.
56. Darwin A, Tormay P, Page L, Griffiths L, Cole J, (1993) Identification of the formate dehydrogenases and genetic determinants of formate-dependent nitrite reduction by Escherichia coli K12. J Gen Microbiol 139: 1829-1840.
57. Rolfe MD, Beek Ter A, Graham AI, Trotter EW, Asif HMS, et al. (2011) Transcript profiling and inference of Escherichia coli K-12 ArcA activity across the range of physiologically relevant oxygen concentrations. J Biol Chem 286: 10147-10154.
58. Sawers G, Heider J, Zehelein E, Böck A, (1991) Expression and operon structure of the sel genes of Escherichia coli and identification of a third selenium-containing formate dehydrogenase isoenzyme. J Bacteriol 173: 4983-4993.
59. Enoch HG, Lester RL, (1975) The purification and properties of formate dehydrogenase and nitrate reductase from Escherichia coli. J Biol Chem 250: 6693-6705.
60. Self WT, Grunden AM, Hasona A, Shanmugam KT, (1999) Transcriptional regulation of molybdoenzyme synthesis in Escherichia coli in response to molybdenum: ModE-molybdate, a repressor of the modABCD (molybdate transport) operon is a secondary transcriptional activator for the hyc and nar operons. Microbiology 145: 41-55.
61. Pinsent J, (1954) The need for selenite and molybdate in the formation of formic dehydrogenase by members of the coli-aerogenes group of bacteria. Biochem J 57: 10-16.
62. Lüke I, Butland G, Moore K, Buchanan G, Lyall V, et al. (2008) Biosynthesis of the respiratory formate dehydrogenases from Escherichia coli: characterization of the FdhE protein. Arch Microbiol 190: 685-696.
63. Mandrand-Berthelot MA, Couchoux-Luthaud G, Santini CL, Giordano G, (1988) Mutants of Escherichia coli specifically deficient in respiratory formate dehydrogenase activity. J Gen Microbiol 134: 3129-3139.
64. Butland G, Peregrín-Alvarez JM, Li J, Yang W, Yang X, et al. (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433: 531-537.
65. Andreini C, Bertini I, Rosato A, (2009) Metalloproteomes: a bioinformatic approach. Acc Chem Res 42: 1471-1479.
66. Cvetkovic A, Menon AL, Thorgersen MP, Scott JW, Poole FL Ii, et al. (2010) Microbial metalloproteomes are largely uncharacterized. Nature 466: 779-782.
67. Salmon K, Hung S-P, Mekjian K, Baldi P, Hatfield GW, et al. (2003) Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J Biol Chem 278: 29837-29855.
68. Constantinidou C, Hobman JL, Griffiths L, Patel MD, Penn CW, et al. (2006) A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J Biol Chem 281: 4802-4815.
69. McDaniel LE, Bailey EG, (1969) Effect of shaking speed and type of closure on shake flask cultures. Appl Microbiol 17: 286-290.
70. Holt JG, (1989) Bergey's manual of systematic bacteriology Lippincott Williams & Wilkins.
71. Zbell AL, Maier RJ, (2009) Role of the Hya hydrogenase in recycling of anaerobically produced H2 in Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 75: 1456-1459.
72. Olson JW, Maier RJ, (2002) Molecular hydrogen as an energy source for Helicobacter pylori. Science 298: 1788-1790.
73. Goodman TG, Hoffman PS, (1983) Hydrogenase activity in catalase-positive strains of Campylobacter spp. J Clin Microbiol 18: 825-829.
74. Shaw DJ, Guest JR, (1982) Amplification and product identification of the fnr gene of Escherichia coli. J Gen Microbiol 128: 2221-2228.
75. Waegeman H, Beauprez J, Moens H, Maertens J, De Mey M, et al. (2011) Effect of iclR and arcA knockouts on biomass formation and metabolic fluxes in Escherichia coli K12 and its implications on understanding the metabolism of Escherichia coli BL21 (DE3). BMC Microbiol 11: 70.
76. Sawers G, (1999) The aerobic/anaerobic interface. Curr Opin Microbiol 2: 181-187.
77. Miller J, (1972) Experiments in Molecular Genetics.
78. Guest JR, (1969) Biochemical and genetic studies with nitrate reductase C-gene mutants of Escherichia coli. Mol Gen Genet 105: 285-297.
79. Begg Y, Whyte J, Haddock B, (1977) The identification of mutants of Escherichia coli deficient in formate dehydrogenase and nitrate reductase activities using dye indicator plates. FEMS Microbiol Lett 2: 47-50.
80. Sambrook J, Russell D, (2001) Molecular Cloning: A Laboratory Manual.
81. Datsenko K, Wanner B, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
82. Hesslinger C, Fairhurst S, Sawers G, (1998) Novel keto acid formate-lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L-threonine to propionate. Mol Microbiol 27: 477-492.
83. Mandrand-Berthelot M-A, Wee M, Haddock B, (1978) An improved method for the Identification and Characterization of Mutants of Escherichia coli deficient in formate dehydrogenase activity. FEMS Microbiol Lett 4: 37-40.
84. Lester RL, DeMoss JA, (1971) Effects of molybdate and selenite on formate and nitrate metabolism in Escherichia coli. J Bacteriol 105: 1006-1014.
85. Lowry O, Rosebrough N, Farr A, Randall R, (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
86. Laemmli U, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
87. Towbin H, Staehelin T, Gordon J, (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76: 4350-4354.
88. Magalon A, Böck A, (2000) Dissection of the maturation reactions of the [NiFe] hydrogenase 3 from Escherichia coli taking place after nickel incorporation. FEBS Lett 473: 254-258.
89. Casadaban MJ, (1976) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104: 541-555.
90. Kaiser M, Sawers G, (1994) Pyruvate formate-lyase is not essential for nitrate respiration by Escherichia coli. FEMS Microbiol Lett 117: 163-168.
91. Balbás P, Soberon X, Merino E, Zurita M, Lomeli H, et al. (1986) Plasmid vector pBR322 and its special-purpose derivatives-a review. Gene 50: 3-40.
92. Self W, Hasona A, Shanmugam K, (2004) Expression and regulation of a silent operon, hyf, coding for hydrogenase 4 isoenzyme in Escherichia coli. J Bacteriol 186: 580-587.