1887

Abstract

Two of the three [NiFe]-hydrogenases (Hyd) of have a hydrogen-uptake function in anaerobic metabolism. While Hyd-2 is maximally synthesized when the bacterium grows by fumarate respiration, Hyd-1 synthesis shows a correlation with fermentation of sugar substrates. In an attempt to advance our knowledge on the physiological function of Hyd-1 during fermentative growth, we examined Hyd-1 activity and levels in various derivatives of K-12 MC4100 with specific defects in sugar utilization. MC4100 lacks a functional fructose phosphotransferase system (PTS) and therefore grows more slowly under anaerobic conditions in rich medium in the presence of -fructose compared with -glucose. Growth in the presence of fructose resulted in an approximately 10-fold increase in Hyd-1 levels in comparison with growth under the same conditions with glucose. This increase in the amount of Hyd-1 was not due to regulation at the transcriptional level. Reintroduction of a functional -encoded fructose PTS into MC4100 restored growth on -fructose and reduced Hyd-1 levels to those observed after growth on -glucose. Reducing the rate of glucose uptake by introducing a mutation in the gene encoding the cAMP receptor protein, or consumption through glycolysis, by introducing a mutation in phosphoglucose isomerase, increased Hyd-1 levels during growth on glucose. These results suggest that the ability to oxidize hydrogen by Hyd-1 shows a strong correlation with the rate of carbon flow through glycolysis and provides a direct link between hydrogen, carbon and energy metabolism.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.056622-0
2012-03-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/3/856.html?itemId=/content/journal/micro/10.1099/mic.0.056622-0&mimeType=html&fmt=ahah

References

  1. Abràmoff M., Magalhaes P., Ram S.. ( 2004;). Image processing with ImageJ. Biophotonics International11:36–42
    [Google Scholar]
  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 Prog15:140–145 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol179:2141–2146[PubMed]
    [Google Scholar]
  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 Biol2:2006–, 0008 [CrossRef][PubMed]
    [Google Scholar]
  5. Ballantine S. P., Boxer D. H.. ( 1985;). Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. J Bacteriol163:454–459[PubMed]
    [Google Scholar]
  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 Biochem156:277–284 [CrossRef][PubMed]
    [Google Scholar]
  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 Lett2:47–50 [CrossRef]
    [Google Scholar]
  8. Böck A., King P. W., Blokesch M., Posewitz M. C.. ( 2006;). Maturation of hydrogenases. Adv Microb Physiol51:1–71 [CrossRef][PubMed]
    [Google Scholar]
  9. Brøndsted L., Atlung T.. ( 1994;). Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli. J Bacteriol176:5423–5428[PubMed]
    [Google Scholar]
  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 Biol104:541–555 [CrossRef][PubMed]
    [Google Scholar]
  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 A97:6640–6645 [CrossRef][PubMed]
    [Google Scholar]
  12. Deutscher J., Francke C., Postma P. W.. ( 2006;). How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev70:939–1031 [CrossRef][PubMed]
    [Google Scholar]
  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 Energy27:1413–1420 [CrossRef]
    [Google Scholar]
  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 J132:341–347[PubMed]
    [Google Scholar]
  15. Forzi L., Sawers R. G.. ( 2007;). Maturation of [NiFe]-hydrogenases in Escherichia coli. Biometals20:565–578 [CrossRef][PubMed]
    [Google Scholar]
  16. Fraenkel D. G.. ( 1996;). Glycolysis. EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  17. Fritsch J., Scheerer P., Frielingsdorf S., Kroschinsky S., Friedrich B., Lenz O., Spahn C. M. T.. ( 2011;). The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron–sulphur centre. Nature479:249–252 [CrossRef][PubMed]
    [Google Scholar]
  18. Giel J. L., Rodionov D., Liu M., Blattner F. R., Kiley P. J.. ( 2006;). IscR-dependent gene expression links iron–sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol Microbiol60:1058–1075 [CrossRef][PubMed]
    [Google Scholar]
  19. Griffith K. L., Wolf R. E. Jr. ( 2002;). Measuring β-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. Biochem Biophys Res Commun290:397–402 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol7:53 [CrossRef][PubMed]
    [Google Scholar]
  21. Jamieson D. J., Higgins C. F.. ( 1986;). Two genetically distinct pathways for transcriptional regulation of anaerobic gene expression in Salmonella typhimurium. J Bacteriol168:389–397[PubMed]
    [Google Scholar]
  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 Rev6:383–398 [CrossRef][PubMed]
    [Google Scholar]
  23. Kornberg H. L.. ( 2001;). Routes for fructose utilization by Escherichia coli. J Mol Microbiol Biotechnol3:355–359[PubMed]
    [Google Scholar]
  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 A97:1808–1812 [CrossRef][PubMed]
    [Google Scholar]
  25. Laemmli U. K.. ( 1970;). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol178:437–442 [CrossRef][PubMed]
    [Google Scholar]
  27. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J.. ( 1951;). Protein measurement with the Folin phenol reagent. J Biol Chem193:265–275[PubMed]
    [Google Scholar]
  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 Chem285:3928–3938 [CrossRef][PubMed]
    [Google Scholar]
  29. Miller J.. ( 1972;). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  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 ONE5:e10132 [CrossRef][PubMed]
    [Google Scholar]
  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 plasmid-bearing Escherichia coli alters metabolic gene expression and improves growth rate. J Biotechnol131:261–269 [CrossRef][PubMed]
    [Google Scholar]
  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 Chem277:49945–49951 [CrossRef][PubMed]
    [Google Scholar]
  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 Bacteriol185:2017–2021 [CrossRef][PubMed]
    [Google Scholar]
  34. Pinske C., Sawers G.. ( 2011;). Iron restriction induces preferential down-regulation of H2-consuming over H2-evolving reactions during fermentative growth of Escherichia coli. BMC Microbiol11:196 [CrossRef][PubMed]
    [Google Scholar]
  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 Microbiol193:893–903 [CrossRef][PubMed]
    [Google Scholar]
  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 Biol217:661–679 [CrossRef][PubMed]
    [Google Scholar]
  37. Postma P. W., Lengeler J. W., Jacobson G. R.. ( 1993;). Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev57:543–594[PubMed]
    [Google Scholar]
  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 Microbiol16:1157–1169 [CrossRef][PubMed]
    [Google Scholar]
  39. Reiner A. M.. ( 1977;). Xylitol and d-arabitol toxicities due to derepressed fructose, galactitol, and sorbitol phosphotransferases of Escherichia coli. J Bacteriol132:166–173[PubMed]
    [Google Scholar]
  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 Lett118:159–162 [CrossRef][PubMed]
    [Google Scholar]
  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. Microbiology145:2903–2912[PubMed]
    [Google Scholar]
  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 Microbiol5:2807–2814 [CrossRef][PubMed]
    [Google Scholar]
  43. Saier M. H. Jr, Ramseier T. M.. ( 1996;). The catabolite repressor/activator (Cra) protein of enteric bacteria. J Bacteriol178:3411–3417[PubMed]
    [Google Scholar]
  44. Sambrook J., Russell D.. ( 2001;). Molecular Cloning: A Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  45. Sauter M., Böhm R., Böck A.. ( 1992;). Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol6:1523–1532 [CrossRef][PubMed]
    [Google Scholar]
  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 Biochem156:265–275 [CrossRef][PubMed]
    [Google Scholar]
  47. Sawers R. G., Clark D.. ( 2004;). Fermentative pyruvate and acetyl-coenzyme A metabolism. EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. Neidhardt F. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  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 Bacteriol164:1324–1331[PubMed]
    [Google Scholar]
  49. Sawers G., Hesslinger C., Muller N., Kaiser M.. ( 1998;). The glycyl radical enzyme TdcE can replace pyruvate formate-lyase in glucose fermentation. J Bacteriol180:3509–3516[PubMed]
    [Google Scholar]
  50. Schlensog V., Lutz S., Böck A.. ( 1994;). Purification and DNA-binding properties of FHLA, the transcriptional activator of the formate hydrogenlyase system from Escherichia coli. J Biol Chem269:19590–19596[PubMed]
    [Google Scholar]
  51. Simons R. W., Houman F., Kleckner N.. ( 1987;). Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene53:85–96 [CrossRef][PubMed]
    [Google Scholar]
  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 A76:4350–4354 [CrossRef][PubMed]
    [Google Scholar]
  53. Varenne S., Casse F., Chippaux M., Pascal M. C.. ( 1975;). A mutant of Escherichia coli deficient in pyruvate formate lyase. Mol Gen Genet141:181–184 [CrossRef][PubMed]
    [Google Scholar]
  54. Zbell A. L., Maier R. J.. ( 2009;). Role of the Hya hydrogenase in recycling of anaerobically produced H2 in Salmonella enterica serovar Typhimurium. Appl Environ Microbiol75:1456–1459 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.056622-0
Loading
/content/journal/micro/10.1099/mic.0.056622-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error