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PMID: 10940038 Published · ppublish English Journal Article

Effects of limited aeration and of the ArcAB system on intermediary pyruvate catabolism in Escherichia coli.

Journal of bacteriology ·Vol. 182 ·No. 17 ·2000-09-00 ·Pages 4934-40

Alexeeva S, de Kort B, Sawers G, Hellingwerf KJ, de Mattos MJ

Abstract

The capacity of Escherichia coli to adapt its catabolism to prevailing redox conditions resides mainly in three catabolic branch points involving (i) pyruvate formate-lyase (PFL) and the pyruvate dehydrogenase complex (PDHc), (ii) the exclusively fermentative enzymes and those of the Krebs cycle, and (iii) the alternative terminal cytochrome bd and cytochrome bo oxidases. A quantitative analysis of the relative catabolic fluxes through these pathways is presented for steady-state glucose-limited chemostat cultures with controlled oxygen availability ranging from full aerobiosis to complete anaerobiosis. Remarkably, PFL contributed significantly to the catabolic flux under microaerobic conditions and was found to be active simultaneously with PDHc and cytochrome bd oxidase-dependent respiration. The synthesis of PFL and cytochrome bd oxidase was found to be maximal in the lower microaerobic range but not in a delta ArcA mutant, and we conclude that the Arc system is more active with respect to regulation of these two positively regulated operons during microaerobiosis than during anaerobiosis.

MeSH Terms
Acetyltransferases/metabolism Bacterial Outer Membrane Proteins/genetics,metabolism Cytochrome b Group Cytochromes/metabolism Electron Transport Chain Complex Proteins Escherichia coli/genetics,growth & development,metabolism Escherichia coli Proteins Glucose/metabolism Membrane Proteins/genetics,metabolism NAD/metabolism Oxidoreductases/metabolism Oxygen/metabolism Protein Kinases/genetics,metabolism Pyruvic Acid/metabolism Repressor Proteins
Chemicals
Bacterial Outer Membrane Proteins Cytochrome b Group Cytochromes Electron Transport Chain Complex Proteins Escherichia coli Proteins Membrane Proteins Repressor Proteins arcA protein, E coli NAD Pyruvic Acid Oxidoreductases cytochrome bd terminal oxidase complex, E coli Acetyltransferases formate C-acetyltransferase Protein Kinases arcB protein, E coli Glucose Oxygen
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Alexeeva S
EC Slater Institute, University of Amsterdam, 1018 WS Amsterdam, The Netherlands.
de Kort B
Sawers G
Hellingwerf K J
de Mattos M J
References (55)
55 references, click to expand
  1. Regulation of pyruvate dehydrogenase complex synthesis in Escherichia coli K 12. Identification of the inducing metabolite.
    Eur J Biochem. 1970 Jun;14(2):258-69 PMID: 4918556
  2. The free radical in pyruvate formate-lyase is located on glycine-734.
    Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):996-1000 PMID: 1310545
  3. The 503-nm pigment of Escherichia coli B: characterization and nutritional conditions affecting its accumulation.
    J Bacteriol. 1973 Feb;113(2):914-21 PMID: 4570612
  4. Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli.
    J Bacteriol. 1978 Apr;134(1):115-24 PMID: 25879
  5. Aerotaxis in Salmonella typhimurium: role of electron transport.
    J Bacteriol. 1981 Feb;145(2):990-1001 PMID: 6257658
  6. Effects of aerobiosis and nitrogen source on the proton motive force in growing Escherichia coli and Klebsiella pneumoniae cells.
    J Bacteriol. 1981 Apr;146(1):377-84 PMID: 6260744
  7. 2-Oxoacid dehydrogenase complexes of Escherichia coli: cellular amounts and patterns of synthesis.
    J Bacteriol. 1983 Oct;156(1):81-8 PMID: 6311808
  8. Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems.
    J Biol Chem. 1984 Mar 10;259(5):3375-81 PMID: 6321507
  9. Transcription analysis of the sucAB, aceEF and lpd genes of Escherichia coli.
    Mol Gen Genet. 1985;200(1):145-54 PMID: 3897791
  10. The cytochrome d complex is a coupling site in the aerobic respiratory chain of Escherichia coli.
    J Biol Chem. 1985 Nov 15;260(26):14003-8 PMID: 2414286
  11. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain.
    Biochemistry. 1987 Dec 1;26(24):7732-7 PMID: 3122832
  12. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1888-92 PMID: 2964639
  13. Anaerobic regulation of pyruvate formate-lyase from Escherichia coli K-12.
    J Bacteriol. 1988 Nov;170(11):5330-6 PMID: 3053657
  14. A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli.
    J Bacteriol. 1989 Feb;171(2):868-73 PMID: 2644240
  15. Phosphotransfer circuitry of the putative multi-signal transducer, ArcB, of Escherichia coli: in vitro studies with mutants.
    Mol Microbiol. 1995 Dec;18(5):953-62 PMID: 8825099
  16. The cytochrome bd quinol oxidase in Escherichia coli has an extremely high oxygen affinity and two oxygen-binding haems: implications for regulation of activity in vivo by oxygen inhibition.
    Microbiology. 1996 Apr;142 ( Pt 4):755-63 PMID: 8936304
  17. Flux analysis and control of the central metabolic pathways in Escherichia coli.
    FEMS Microbiol Rev. 1996 Dec;19(2):85-116 PMID: 8988566
  18. Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidase (cyoABCDE and cydAB) genes in Escherichia coli.
    FEMS Microbiol Lett. 1992 Feb 1;70(1):31-6 PMID: 1315704
  19. Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins.
    J Bacteriol. 1992 Jun;174(11):3474-8 PMID: 1592804
  20. Purification and phosphorylation of the Arc regulatory components of Escherichia coli.
    J Bacteriol. 1992 Sep;174(17):5617-23 PMID: 1512197
  21. Experimental conditions may affect reproducibility of the beta-galactosidase assay.
    FEMS Microbiol Lett. 1992 Dec 15;100(1-3):87-90 PMID: 1478485
  22. Energetic efficiency of Escherichia coli: effects of mutations in components of the aerobic respiratory chain.
    J Bacteriol. 1993 May;175(10):3020-5 PMID: 8491720
  23. Adaptation of Escherichia coli to redox environments by gene expression.
    Mol Microbiol. 1993 Jul;9(1):9-15 PMID: 8412675
  24. Phosphorylation/dephosphorylation of the receiver module at the conserved aspartate residue controls transphosphorylation activity of histidine kinase in sensor protein ArcB of Escherichia coli.
    J Biol Chem. 1993 Nov 15;268(32):23972-80 PMID: 8226939
  25. Differences in sensitivity to NADH of purified pyruvate dehydrogenase complexes of Enterococcus faecalis, Lactococcus lactis, Azotobacter vinelandii and Escherichia coli: implications for their activity in vivo.
    FEMS Microbiol Lett. 1993 Dec 15;114(3):279-83 PMID: 8288104
  26. Effect of oxygen on ethanol production by a recombinant ethanologenic E. coli.
    Appl Biochem Biotechnol. 1994 Spring;45-46:349-66 PMID: 8010765
  27. Isolation and characterization of hypophosphite--resistant mutants of Escherichia coli: identification of the FocA protein, encoded by the pfl operon, as a putative formate transporter.
    Mol Microbiol. 1994 Mar;11(5):965-82 PMID: 8022272
  28. Induction of the Escherichia coli cytochrome d by low delta mu H+ and by sodium ions.
    Eur J Biochem. 1995 Aug 15;232(1):304-8 PMID: 7556165
  29. Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli.
    J Bacteriol. 1996 Feb;178(4):1094-8 PMID: 8576043
  30. Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments.
    J Biochem. 1996 Dec;120(6):1055-63 PMID: 9010748
  31. Insights into multistep phosphorelay from the crystal structure of the C-terminal HPt domain of ArcB.
    Cell. 1997 Mar 7;88(5):717-23 PMID: 9054511
  32. In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli.
    J Bacteriol. 1997 Sep;179(17):5429-35 PMID: 9286997
  33. Regulatory O2 tensions for the synthesis of fermentation products in Escherichia coli and relation to aerobic respiration.
    Arch Microbiol. 1997 Oct;168(4):290-6 PMID: 9297466
  34. Respiratory protection of nitrogenase activity in Azotobacter vinelandii--roles of the terminal oxidases.
    Biosci Rep. 1997 Jun;17(3):303-17 PMID: 9337485
  35. Environmental control of pyruvate dehydrogenase complex expression in Escherichia coli.
    FEMS Microbiol Lett. 1998 Feb 15;159(2):325-9 PMID: 9503628
  36. A dual-signaling mechanism mediated by the ArcB hybrid sensor kinase containing the histidine-containing phosphotransfer domain in Escherichia coli.
    J Bacteriol. 1998 Aug;180(15):3973-7 PMID: 9683496
  37. The structure and function of the histidine-containing phosphotransfer (HPt) signaling domain of the Escherichia coli ArcB sensor.
    J Biochem. 1998 Aug;124(2):440-5 PMID: 9685739
  38. A glycyl radical solution: oxygen-dependent interconversion of pyruvate formate-lyase.
    Mol Microbiol. 1998 Aug;29(4):945-54 PMID: 9767563
  39. Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system.
    J Biol Chem. 1998 Dec 4;273(49):32864-9 PMID: 9830034
  40. Mutational analysis of the histidine-containing phosphotransfer (HPt) signaling domain of the ArcB sensor in Escherichia coli.
    Biosci Biotechnol Biochem. 1998 Nov;62(11):2236-8 PMID: 9972245
  41. The steady-state internal redox state (NADH/NAD) reflects the external redox state and is correlated with catabolic adaptation in Escherichia coli.
    J Bacteriol. 1999 Apr;181(8):2351-7 PMID: 10197995
  42. PAS domains: internal sensors of oxygen, redox potential, and light.
    Microbiol Mol Biol Rev. 1999 Jun;63(2):479-506 PMID: 10357859
  43. Agitation-aeration in the laboratory and in industry.
    Bacteriol Rev. 1954 Dec;18(4):254-74 PMID: 13219049
  44. Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons.
    Res Microbiol. 1994 Jun-Aug;145(5-6):437-50 PMID: 7855430
  45. Purification of NADH-ferricyanide dehydrogenase and NADH-quinone reductase from Escherichia coli membranes and their roles in the respiratory chain.
    Biochim Biophys Acta. 1989 Oct 26;977(1):62-9 PMID: 2679883
  46. The fermentation pathways of Escherichia coli.
    FEMS Microbiol Rev. 1989 Sep;5(3):223-34 PMID: 2698228
  47. The arcB gene of Escherichia coli encodes a sensor-regulator protein for anaerobic repression of the arc modulon.
    Mol Microbiol. 1990 May;4(5):715-27 PMID: 2201868
  48. Involvement of pyruvate dehydrogenase in product formation in pyruvate-limited anaerobic chemostat cultures of Enterococcus faecalis NCTC 775.
    Arch Microbiol. 1990;154(1):50-5 PMID: 2118752
  49. Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli: study utilizing deletions and lac fusions of cyo and cyd.
    J Bacteriol. 1990 Oct;172(10):6020-5 PMID: 2170337
  50. Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product.
    J Bacteriol. 1990 Nov;172(11):6333-8 PMID: 2172211
  51. FNR and its role in oxygen-regulated gene expression in Escherichia coli.
    FEMS Microbiol Rev. 1990 Aug;6(4):399-428 PMID: 2248796
  52. Properties of the two terminal oxidases of Escherichia coli.
    Biochemistry. 1991 Apr 23;30(16):3936-42 PMID: 1850294
  53. The requirement of ArcA and Fnr for peak expression of the cyd operon in Escherichia coli under microaerobic conditions.
    Mol Gen Genet. 1991 Apr;226(1-2):209-13 PMID: 1851949
  54. Adaptive responses to oxygen limitation in Escherichia coli.
    Trends Biochem Sci. 1991 Aug;16(8):310-4 PMID: 1957353
  55. The redox environment and microbial physiology. I. The transition from anaerobiosis to aerobiosis in continuous cultures of facultative anaerobes.
    Biochim Biophys Acta. 1971 Dec 7;253(2):352-9 PMID: 4332305
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.182.17.4934-4940.2000
Published
2000-09-00
Pages
4934-40
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC111374
Subset
IM
External Links
PubMed source DOI: 10.1128/JB.182.17.4934-4940.2000 PMC Full Text View journal details
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