Home LiteratureArticle Details
PMID: 8576043 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

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.

Journal of bacteriology ·Vol. 178 ·No. 4 ·1996-02-00 ·Pages 1094-8

Tseng CP, Albrecht J, Gunsalus RP

Abstract

Escherichia coli varies the synthesis of many of its respiratory enzymes in response to oxygen availability. These enzymes include cytochrome o oxidase (cyoABCDE) and cytochrome d oxidase (cydAB), used during aerobic cell growth, and a fumarate reductase (frdABCD), dimethyl sulfoxide/trimethylamine oxide reductase (dmsABC), and nitrate reductase (narGHJI), used during anaerobic respiratory conditions. To determine how different levels of oxygen affect the expression of each operon, strains containing cyo-lacZ, cyd-lacZ, frdA-lacZ, dmsA-lacZ, and narG-lacZ fusions were grown in continuous culture at various degrees of air saturation. The basal-level expression of the anaerobic respiratory genes, frdABCD, dmsABC, and narGHJI, occurred when the air saturation of the medium was above 20%; as the saturation was reduced to below 10% (ca. 2% oxygen), the expression rapidly increased and reached a maximal level at 0% air. In contrast, cyoABCDE gene expression was lowest under anaerobic conditions while cyd-lacZ expression was about 40% of its maximum level. When the oxygen level was raised into the microaerophilic range (ca. 7% air saturation) cyd-lacZ expression was maximal while cyo-lacZ expression was elevated by about fivefold. As the air level was raised to above 20% saturation, cyd-lacZ expression fell to a basal level while cyo-lacZ expression was increased to its maximum level. The role of the Fnr and ArcA regulatory proteins in this microaerophilic control of respiratory gene expression was documented: whereas Fnr function as an aerobic/anaerobic switch in the range of 0 to 10% air saturation, ArcA exerted its control in the 10 to 20% range. These two transcriptional regulators coordinate the hierarchial control of respiratory pathway gene expression in E. coli to ensure the optimal use of oxygen in the cell environment.

MeSH Terms
Aerobiosis Anaerobiosis Bacterial Outer Membrane Proteins/metabolism Bacterial Proteins/metabolism Cytochrome b Group Cytochromes/biosynthesis Electron Transport Chain Complex Proteins Electron Transport Complex IV/biosynthesis Escherichia coli/drug effects,genetics,physiology Escherichia coli Proteins Gene Expression Regulation, Bacterial Iron-Sulfur Proteins NADH, NADPH Oxidoreductases/biosynthesis Nitrate Reductase Nitrate Reductases/biosynthesis Oxidoreductases/biosynthesis Oxidoreductases Acting on CH-NH Group Donors Oxygen/pharmacology Recombinant Fusion Proteins/biosynthesis Repressor Proteins Succinate Dehydrogenase/biosynthesis
Chemicals
Bacterial Outer Membrane Proteins Bacterial Proteins Cytochrome b Group Cytochromes Electron Transport Chain Complex Proteins Escherichia coli Proteins FNR protein, E coli Iron-Sulfur Proteins Recombinant Fusion Proteins Repressor Proteins arcA protein, E coli Oxidoreductases Succinate Dehydrogenase methylamine dehydrogenase Oxidoreductases Acting on CH-NH Group Donors NADH, NADPH Oxidoreductases Nitrate Reductases Nitrate Reductase dimethyl sulfoxide reductase cytochrome bd terminal oxidase complex, E coli cytochrome o oxidase Electron Transport Complex IV Oxygen
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Tseng C P
Department of Microbiology and Molecular Genetics, University of California, Los Angeles 90095, USA.
Albrecht J
Gunsalus R P
References (18)
18 references, click to expand
  1. Oxygen-limited continuous culture and respiratory energy conservation in Escherichia coli.
    J Bacteriol. 1978 Apr;134(1):115-24 PMID: 25879
  2. 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
  3. 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
  4. Oxygen, nitrate, and molybdenum regulation of dmsABC gene expression in Escherichia coli.
    J Bacteriol. 1989 Jul;171(7):3817-23 PMID: 2544558
  5. 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
  6. 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
  7. Mutations in fnr that alter anaerobic regulation of electron transport-associated genes in Escherichia coli.
    J Biol Chem. 1990 Nov 5;265(31):18733-6 PMID: 2229038
  8. FNR and its role in oxygen-regulated gene expression in Escherichia coli.
    FEMS Microbiol Rev. 1990 Aug;6(4):399-428 PMID: 2248796
  9. 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
  10. Adaptation of Escherichia coli to respiratory conditions: regulation of gene expression.
    Cell. 1991 Jul 12;66(1):5-7 PMID: 2070418
  11. Oxygen regulated gene expression in Escherichia coli: control of anaerobic respiration by the FNR protein.
    Antonie Van Leeuwenhoek. 1991 Feb;59(2):65-76 PMID: 1854188
  12. 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
  13. Purification and phosphorylation of the Arc regulatory components of Escherichia coli.
    J Bacteriol. 1992 Sep;174(17):5617-23 PMID: 1512197
  14. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes.
    J Bacteriol. 1992 Nov;174(22):7069-74 PMID: 1331024
  15. Activation of the Escherichia coli nitrate reductase (narGHJI) operon by NarL and Fnr requires integration host factor.
    J Biol Chem. 1993 Jan 15;268(2):771-4 PMID: 8419352
  16. 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
  17. Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli.
    J Bacteriol. 1994 Nov;176(21):6599-605 PMID: 7961411
  18. Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product.
    J Bacteriol. 1987 Jul;169(7):3340-9 PMID: 3298218
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-02-00
Pages
1094-8
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC177770
Subset
IM
Grants
NIAID NIH HHS · AI21678 · United States
NIGMS NIH HHS · GM49694 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]