Analysis of hydrogenase 1 levels reveals an intimate link between carbon and hydrogen metabolism in Escherichia coli K-12

Microbiology

Volumn 158, Issue 3, 2012, Pages 856-868

  Pinske, Constanze ^a   McDowall, Jennifer S ^b   Sargent, Frank ^b   Gary Sawers, R ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; CYCLIC AMP RECEPTOR; FRUCTOSE; FRUCTOSE PHOSPHOTRANSFERASE; FUMARIC ACID; GLUCOSE; GLUCOSE 6 PHOSPHATE ISOMERASE; HYDROGEN; NICKEL IRON HYDROGENASE; UNCLASSIFIED DRUG;

ANAEROBIC METABOLISM; ARTICLE; CARBON METABOLISM; ENERGY METABOLISM; ENZYME ANALYSIS; ESCHERICHIA COLI K 12; GENE MUTATION; GLUCOSE TRANSPORT; GLYCOLYSIS; PRIORITY JOURNAL;

ANAEROBIOSIS; CARBON; CULTURE MEDIA; ENERGY METABOLISM; ESCHERICHIA COLI K12; FERMENTATION; FRUCTOSE; GLUCOSE; HYDROGEN; METABOLIC NETWORKS AND PATHWAYS; OXIDOREDUCTASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 84857768182     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.056622-0     Document Type: Article

References (54)

1. Abràmoff, M., Magalhaes, P. & Ram, S. (2004). Image processing with ImageJ. Biophotonics International 11, 36-42.
2. Aristidou, A. A., San, K. Y. & Bennett, G. N. (1999). Improvement of biomass yield and recombinant gene expression in Escherichia coli by using fructose as the primary carbon source. Biotechnol Prog 15, 140-145.
3. Atlung, T., Knudsen, K., Heerfordt, L. & Brøndsted, L. (1997). Effects of sigmaS and the transcriptional activator AppY on induction of the Escherichia coli hya and cbdAB-appA operons in response to carbon and phosphate starvation. J Bacteriol 179, 2141-2146.
4. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L. & Mori, H. (2006). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 2006, 0008.
5. Ballantine, S. P. & Boxer, D. H. (1985). Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J Bacteriol 163, 454-459.
6. Ballantine, S. P. & Boxer, D. H. (1986). Isolation and characterisation of a soluble active fragment of hydrogenase isoenzyme 2 from the membranes of anaerobically grown Escherichia coli. Eur J Biochem 156, 277-284.
7. 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.
8. Böck, A., King, P. W., Blokesch, M. & Posewitz, M. C. (2006). Maturation of hydrogenases. Adv Microb Physiol 51, 1-71.
9. Brøndsted, L. & Atlung, T. (1994). Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli. J Bacteriol 176, 5423-5428.
10. Casadaban, M. J. (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.
11. Datsenko, K. A. & Wanner, B. L. (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.
12. Deutscher, J., Francke, C. & Postma, P. W. (2006). How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70, 939-1031.
13. Dubini, A., Pye, R., Jack, R., Palmer, T. & Sargent, F. (2002). How bacteria get energy from hydrogen: a genetic analysis of periplasmic hydrogen oxidation in Escherichia coli. Int J Hydrogen Energy 27, 1413-1420.
14. Ferenci, T. & Kornberg, H. L. (1973). The utilization of fructose by Escherichia coli. Properties of a mutant defective in fructose 1-phosphate kinase activity. Biochem J 132, 341-347.
15. Forzi, L. & Sawers, R. G. (2007). Maturation of [NiFe]-hydrogenases in Escherichia coli. Biometals 20, 565-578.
16. Fraenkel, D. G. (1996). Glycolysis. In EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Edited by F. C. Neidhardt. Washington, DC: American Society for Microbiology.
17. Fritsch, J., Scheerer, P., Frielingsdorf, S., Kroschinsky, S., Friedrich, B., Lenz, O. & Spahn, C. M. T. (2011). The crystal structure of an oxygentolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479, 249-252.
18. 2-regulated genes in Escherichia coli. Mol Microbiol 60, 1058-1075.
19. Griffith, K. L. & Wolf, R. E., Jr (2002). Measuring b-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. Biochem Biophys Res Commun 290, 397-402.
20. Gutierrez-Ríos, R. M., Freyre-Gonzalez, J. A., Resendis, O., Collado-Vides, J., Saier, M. & Gosset, G. (2007). Identification of regulatory network topological units coordinating the genome-wide transcriptional response to glucose in Escherichia coli. BMC Microbiol 7, 53.
21. Jamieson, D. J. & Higgins, C. F. (1986). Two genetically distinct pathways for transcriptional regulation of anaerobic gene expression in Salmonella typhimurium. J Bacteriol 168, 389-397.
22. Knappe, J. & Sawers, G. (1990). A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli. FEMS Microbiol Rev 6, 383-398.
23. Kornberg, H. L. (2001). Routes for fructose utilization by Escherichia coli. J Mol Microbiol Biotechnol 3, 355-359.
24. Kornberg, H. L., Lambourne, L. T. & Sproul, A. A. (2000). Facilitated diffusion of fructose via the phosphoenolpyruvate/glucose phosphotransferase system of Escherichia coli. Proc Natl Acad Sci U S A 97, 1808-1812.
25. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
26. Laurinavichene, T. V., Zorin, N. A. & Tsygankov, A. A. (2002). Effect of redox potential on activity of hydrogenase 1 and hydrogenase 2 in Escherichia coli. Arch Microbiol 178, 437-442.
27. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
28. Lukey, M. J., Parkin, A., Roessler, M. M., Murphy, B. J., Harmer, J., Palmer, T., Sargent, F. & Armstrong, F. A. (2010). How Escherichia coli is equipped to oxidize hydrogen under different redox conditions. J Biol Chem 285, 3928-3938.
29. Miller, J. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
30. Noguchi, K., Riggins, D. P., Eldahan, K. C., Kitko, R. D. & Slonczewski, J. L. (2010). Hydrogenase-3 contributes to anaerobic acid resistance of Escherichia coli. PLoS ONE 5, e10132.
31. Ow, D. S.-W., Lee, R. M.-Y., Nissom, P. M., Philp, R., Oh, S. K.-W. & Yap, M. G.-S. (2007). Inactivating FruR global regulator in plasmidbearing Escherichia coli alters metabolic gene expression and improves growth rate. J Biotechnol 131, 261-269.
32. 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.
33. Peters, J. E., Thate, T. E. & Craig, N. L. (2003). Definition of the Escherichia coli MC4100 genome by use of a DNA array. J Bacteriol 185, 2017-2021.
34. 2-evolving reactions during fermentative growth of Escherichia coli. BMC Microbiol 11, 196.
35. Pinske, C., Krüger, S., Soboh, B., Ihling, C., Kuhns, M., Braussemann, M., Jaroschinsky, M., Sauer, C., Sargent, F. & other authors (2011). Efficient electron transfer from hydrogen to benzyl viologen by the [NiFe]-hydrogenases of Escherichia coli is dependent on the coexpression of the iron-sulfur cluster-containing small subunit. Arch Microbiol 193, 893-903.
36. Plumbridge, J. & Kolb, A. (1991). CAP and Nag repressor binding to the regulatory regions of the nagE-B and manX genes of Escherichia coli. J Mol Biol 217, 661-679.
37. Postma, P. W., Lengeler, J. W. & Jacobson, G. R. (1993). Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57, 543-594.
38. Ramseier, T. M., Bledig, S., Michotey, V., Feghali, R. & Saier, M. H., Jr (1995). The global regulatory protein FruR modulates the direction of carbon flow in Escherichia coli. Mol Microbiol 16, 1157-1169.
39. Reiner, A. M. (1977). Xylitol and D-arabitol toxicities due to derepressed fructose, galactitol, and sorbitol phosphotransferases of Escherichia coli. J Bacteriol 132, 166-173.
40. Reizer, J., Reizer, A., Kornberg, H. L. & Saier, M. H., Jr (1994). Sequence of the fruB gene of Escherichia coli encoding the diphosphoryl transfer protein (DTP) of the phosphoenolpyruvate: sugar phosphotransferase system. FEMS Microbiol Lett 118, 159-162.
41. Richard, D. J., Sawers, G., Sargent, F., McWalter, L. & Boxer, D. H. (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.
42. 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.
43. Saier, M. H., Jr & Ramseier, T. M. (1996). The catabolite repressor/activator (Cra) protein of enteric bacteria. J Bacteriol 178, 3411-3417.
44. Sambrook, J. & Russell, D. (2001). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
45. 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.
46. Sawers, R. G. & Boxer, D. H. (1986). Purification and properties of membrane-bound hydrogenase isoenzyme 1 from anaerobically grown Escherichia coli K12. Eur J Biochem 156, 265-275.
47. Sawers, R. G. & Clark, D. (2004). Fermentative pyruvate and acetylcoenzyme A metabolism. In EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Edited by F. C. Neidhardt. Washington, DC: American Society for Microbiology.
48. Sawers, R. G., Ballantine, S. P. & Boxer, D. H. (1985). Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzyme. J Bacteriol 164, 1324-1331.
49. Sawers, G., Hesslinger, C., Muller, N. & Kaiser, M. (1998). The glycyl radical enzyme TdcE can replace pyruvate formate-lyase in glucose fermentation. J Bacteriol 180, 3509-3516.
50. Schlensog, V., Lutz, S. & Böck, A. (1994). Purification and DNA-binding properties of FHLA, the transcriptional activator of the formate hydrogenlyase system fromEscherichia coli. J Biol Chem269, 19590-19596.
51. Simons, R. W., Houman, F. & Kleckner, N. (1987). Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53, 85-96.
52. 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.
53. Varenne, S., Casse, F., Chippaux, M. & Pascal, M. C. (1975). A mutant of Escherichia coli deficient in pyruvate formate lyase. Mol Gen Genet 141, 181-184.
54. 2 in Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 75, 1456-1459.