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PMID: 12511500 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

FlhD/FlhC is a regulator of anaerobic respiration and the Entner-Doudoroff pathway through induction of the methyl-accepting chemotaxis protein Aer.

Journal of bacteriology ·Vol. 185 ·No. 2 ·2003-01-00 ·Pages 534-43

Prüss BM, Campbell JW, Van Dyk TK, Zhu C, Kogan Y, Matsumura P

Abstract

The regulation by two transcriptional activators of flagellar expression (FlhD and FlhC) and the chemotaxis methyl-accepting protein Aer was studied with glass slide DNA microarrays. An flhD::Kan insertion and an aer deletion were independently introduced into two Escherichia coli K-12 strains, and the effects upon gene regulation were investigated. Altogether, the flhD::Kan insertion altered the expression of 29 operons of known function. Among them was Aer, which in turn regulated a subset of these operons, namely, the ones involved in anaerobic respiration and the Entner-Doudoroff pathway. In addition, FlhD/FlhC repressed enzymes involved in aerobic respiration and regulated many other metabolic enzymes and transporters in an Aer-independent manner. Expression of 12 genes of uncharacterized function was also affected. FlhD increased gltBD, gcvTHP, and ompT expression. The regulation of half of these genes was subsequently confirmed with reporter gene fusions, enzyme assays, and real-time PCR. Growth phenotypes of flhD and flhC mutants were determined with Phenotype MicroArrays and correlated with gene expression.

MeSH Terms
Anaerobiosis Bacterial Proteins Carrier Proteins/genetics,metabolism Chemotaxis DNA-Binding Proteins/genetics,metabolism Escherichia coli/genetics,metabolism,physiology Escherichia coli Proteins/genetics,metabolism Gene Expression Regulation, Bacterial Intercellular Signaling Peptides and Proteins Membrane Proteins/genetics,metabolism Methyl-Accepting Chemotaxis Proteins Oligonucleotide Array Sequence Analysis/instrumentation,methods Operon Oxygen Consumption Pentose Phosphate Pathway Phosphogluconate Dehydrogenase/genetics,metabolism Trans-Activators/genetics,metabolism
Chemicals
Aer protein, E coli Bacterial Proteins Carrier Proteins DNA-Binding Proteins Escherichia coli Proteins Intercellular Signaling Peptides and Proteins Membrane Proteins Methyl-Accepting Chemotaxis Proteins Trans-Activators flhC protein, E coli flhD protein, E coli Phosphogluconate Dehydrogenase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Prüss Birgit M
Department of Microbiology and Immunology, University of Illinois at Chicago, 60612-7344, USA. pruess@UIC.EDU
Campbell John W
Van Dyk Tina K
Zhu Charles
Kogan Yakov
Matsumura Philip
References (60)
60 references, click to expand
  1. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors.
    Biochim Biophys Acta. 1997 Jul 4;1320(3):217-34 PMID: 9230919
  2. A signal transducer for aerotaxis in Escherichia coli.
    J Bacteriol. 1997 Jun;179(12):4075-9 PMID: 9190831
  3. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior.
    Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10541-6 PMID: 9380671
  4. Regulation of carAB expression in Escherichia coli occurs in part through UTP-sensitive reiterative transcription.
    J Bacteriol. 1998 Feb;180(3):705-13 PMID: 9457878
  5. Constricted flux through the branched-chain amino acid biosynthetic enzyme acetolactate synthase triggers elevated expression of genes regulated by rpoS and internal acidification.
    J Bacteriol. 1998 Feb;180(4):785-92 PMID: 9473030
  6. Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression.
    J Bacteriol. 1998 May;180(9):2442-9 PMID: 9573197
  7. What's for dinner?: Entner-Doudoroff metabolism in Escherichia coli.
    J Bacteriol. 1998 Jul;180(14):3495-502 PMID: 9657988
  8. Sequence analysis of the GntII (subsidiary) system for gluconate metabolism reveals a novel pathway for L-idonic acid catabolism in Escherichia coli.
    J Bacteriol. 1998 Jul;180(14):3704-10 PMID: 9658018
  9. Fnr, NarP, and NarL regulation of Escherichia coli K-12 napF (periplasmic nitrate reductase) operon transcription in vitro.
    J Bacteriol. 1998 Aug;180(16):4192-8 PMID: 9696769
  10. Anaerobic expression of Escherichia coli succinate dehydrogenase: functional replacement of fumarate reductase in the respiratory chain during anaerobic growth.
    J Bacteriol. 1998 Nov;180(22):5989-96 PMID: 9811659
  11. Model of maltose-binding protein/chemoreceptor complex supports intrasubunit signaling mechanism.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):939-44 PMID: 9927672
  12. The cyclic AMP receptor protein is dependent on GcvA for regulation of the gcv operon.
    J Bacteriol. 1999 Mar;181(6):1912-9 PMID: 10074087
  13. Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis.
    J Bacteriol. 1999 Apr;181(7):2209-16 PMID: 10094700
  14. Virulence gene regulation in pathogenic Escherichia coli.
    Vet Res. 1999 Mar-Jun;30(2-3):131-55 PMID: 10367352
  15. Molecular interactions in ribose transport: the binding protein module symmetrically associates with the homodimeric membrane transporter.
    EMBO J. 1999 Aug 2;18(15):4149-56 PMID: 10428954
  16. The napF and narG nitrate reductase operons in Escherichia coli are differentially expressed in response to submicromolar concentrations of nitrate but not nitrite.
    J Bacteriol. 1999 Sep;181(17):5303-8 PMID: 10464201
  17. Glucose and gluconic acid oxidation of Pseudomonas saccharophila.
    J Biol Chem. 1952 May;196(2):853-62 PMID: 12981024
  18. Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli.
    Mol Microbiol. 1993 Aug;9(3):425-34 PMID: 8412692
  19. Mutations in NADH:ubiquinone oxidoreductase of Escherichia coli affect growth on mixed amino acids.
    J Bacteriol. 1994 Apr;176(8):2143-50 PMID: 8157582
  20. The structural basis of sequence-independent peptide binding by OppA protein.
    Science. 1994 Jun 10;264(5165):1578-81 PMID: 8202710
  21. The glucose-starvation stimulon of Escherichia coli: induced and repressed synthesis of enzymes of central metabolic pathways and role of acetyl phosphate in gene expression and starvation survival.
    Mol Microbiol. 1994 Jun;12(5):833-43 PMID: 8052134
  22. Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli.
    Mol Microbiol. 1994 Jun;12(6):973-84 PMID: 7934904
  23. The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons.
    J Bacteriol. 1994 Dec;176(23):7345-51 PMID: 7961507
  24. The dipeptide permease of Escherichia coli closely resembles other bacterial transport systems and shows growth-phase-dependent expression.
    Mol Microbiol. 1994 Dec;14(5):1077-92 PMID: 7536291
  25. Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR.
    J Bacteriol. 1995 Aug;177(16):4696-702 PMID: 7642497
  26. A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division.
    J Bacteriol. 1996 Feb;178(3):668-74 PMID: 8550498
  27. A genomic approach to gene fusion technology.
    Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2555-60 PMID: 11226277
  28. Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response.
    J Bacteriol. 2001 Apr;183(7):2178-86 PMID: 11244055
  29. Manufacturing DNA microarrays of high spot homogeneity and reduced background signal.
    Nucleic Acids Res. 2001 Apr 1;29(7):E38 PMID: 11266573
  30. FlhD/FlhC-regulated promoters analyzed by gene array and lacZ gene fusions.
    FEMS Microbiol Lett. 2001 Apr 1;197(1):91-7 PMID: 11287152
  31. Crystallization and preliminary X-ray crystallographic analysis of Escherichia coli RbsD, a component of the ribose-transport system with unknown biochemical function.
    Acta Crystallogr D Biol Crystallogr. 2001 May;57(Pt 5):728-30 PMID: 11320319
  32. Activation from a distance: roles of Lrp and integration host factor in transcriptional activation of gltBDF.
    J Bacteriol. 2001 Jul;183(13):3910-8 PMID: 11395454
  33. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function.
    Genome Res. 2001 Jul;11(7):1246-55 PMID: 11435407
  34. LuxArray, a high-density, genomewide transcription analysis of Escherichia coli using bioluminescent reporter strains.
    J Bacteriol. 2001 Oct;183(19):5496-505 PMID: 11544210
  35. Acetate and formate stress: opposite responses in the proteome of Escherichia coli.
    J Bacteriol. 2001 Nov;183(21):6466-77 PMID: 11591692
  36. Regulation of expression of the flagellin gene (hag) in Escherichia coli K-12: analysis of hag-lac gene fusions.
    J Bacteriol. 1979 Sep;139(3):721-9 PMID: 113385
  37. D-Amino acid dehydrogenase of Escherichia coli K12: positive selection of mutants defective in enzyme activity and localization of the structural gene.
    Mol Gen Genet. 1981;181(3):373-8 PMID: 6113535
  38. Isolation and characterization of the Fnr protein, the transcriptional regulator of anaerobic electron transport in Escherichia coli.
    Eur J Biochem. 1985 Jan 2;146(1):193-9 PMID: 2981682
  39. Identification of the dadX gene coding for the predominant isozyme of alanine racemase in Escherichia coli K12.
    Mol Gen Genet. 1985;198(2):315-22 PMID: 3920477
  40. 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
  41. Flagellar transcriptional activators FlbB and FlaI: gene sequences and 5' consensus sequences of operons under FlbB and FlaI control.
    J Bacteriol. 1988 Apr;170(4):1575-81 PMID: 2832369
  42. Central metabolism of the archaebacteria: an overview.
    Can J Microbiol. 1989 Jan;35(1):58-64 PMID: 2497944
  43. 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
  44. The tdh and serA operons of Escherichia coli: mutational analysis of the regulatory elements of leucine-responsive genes.
    J Bacteriol. 1991 Oct;173(19):5944-53 PMID: 1917830
  45. Identification of elements involved in transcriptional regulation of the Escherichia coli cad operon by external pH.
    J Bacteriol. 1992 Jan;174(2):530-40 PMID: 1370290
  46. Nucleotide sequence of the Escherichia coli cad operon: a system for neutralization of low extracellular pH.
    J Bacteriol. 1992 Apr;174(8):2659-69 PMID: 1556085
  47. Regulation of the Escherichia coli cad operon: location of a site required for acid induction.
    J Bacteriol. 1992 Apr;174(8):2670-8 PMID: 1556086
  48. Molecular characterization of the Entner-Doudoroff pathway in Escherichia coli: sequence analysis and localization of promoters for the edd-eda operon.
    J Bacteriol. 1992 Jul;174(14):4638-46 PMID: 1624451
  49. Function of the Escherichia coli nucleoid protein, H-NS: molecular analysis of a subset of proteins whose expression is enhanced in a hns deletion mutant.
    Mol Gen Genet. 1993 Feb;237(1-2):113-22 PMID: 8455549
  50. Global regulation of gene expression in Escherichia coli.
    J Bacteriol. 1993 Apr;175(7):2026-36 PMID: 8458845
  51. Roles of the GcvA and PurR proteins in negative regulation of the Escherichia coli glycine cleavage enzyme system.
    J Bacteriol. 1993 Aug;175(16):5129-34 PMID: 8349552
  52. Characterization of the glyceraldehyde 3-phosphate dehydrogenase from the extremely halophilic archaebacterium Haloarcula vallismortis.
    Arch Microbiol. 1993;160(1):5-11 PMID: 8352651
  53. 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
  54. Isolation of an oxygen-sensitive FNR protein of Escherichia coli: interaction at activator and repressor sites of FNR-controlled genes.
    Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1226-31 PMID: 8577745
  55. Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli.
    J Bacteriol. 1996 Aug;178(15):4344-66 PMID: 8755861
  56. Defect in export and synthesis of the periplasmic galactose receptor MglB in dnaK mutants of Escherichia coli, and decreased stability of the mglB mRNA.
    Microbiology. 1996 Sep;142 ( Pt 9):2595-602 PMID: 8828228
  57. Molecular analysis of the gat genes from Escherichia coli and of their roles in galactitol transport and metabolism.
    J Bacteriol. 1996 Dec;178(23):6790-5 PMID: 8955298
  58. Evolution of carbohydrate metabolic pathways.
    Res Microbiol. 1996 Jul-Sep;147(6-7):448-55 PMID: 9084754
  59. The Escherichia coli flagellar transcriptional activator flhD regulates cell division through induction of the acid response gene cadA.
    J Bacteriol. 1997 Jun;179(11):3818-21 PMID: 9171439
  60. Aerobic regulation of cytochrome d oxidase (cydAB) operon expression in Escherichia coli: roles of Fnr and ArcA in repression and activation.
    Mol Microbiol. 1997 Aug;25(3):605-15 PMID: 9302022
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2003-01-00
Pages
534-43
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC145316
Subset
IM
Grants
NIGMS NIH HHS · GM59484 · United States
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