Carbon and energy metabolism of atp mutants of Escherichia coli

Peter Ruhdal Jensen, Ole Michelsen

    Research output: Contribution to journalJournal articleResearchpeer-review

    Abstract

    The membrane-bound H+-ATPase plays a key role in free-energy transduction of biological systems. We report how the carbon and energy metabolism of Escherichia coli changes in response to deletion of the atp operon that encodes this enzyme. Compared with the isogenic wild-type strain, the growth rate and growth yield were decreased less than expected for a shift from oxidative phosphorylation to glycolysis alone as a source of ATP. Moreover, the respiration rate of a atp deletion strain was increased by 40% compared with the wild-type strain. This result is surprising, since the atp deletion strain is not able to utilize the resulting proton motive force for ATP synthesis. Indeed, the ratio of ATP concentration to ADP concentration was decreased from 19 in the wild type to 7 in the atp mutant, and the membrane potential of the atp deletion strain was increased by 20%, confirming that the respiration rate was not controlled by the magnitude of the opposing membrane potential. The level of type b cytochromes in the mutant cells was 80% higher than the level in the wild-type cells, suggesting that the increased respiration was caused by an increase in the expression of the respiratory genes. The atp deletion strain produced twice as much by-product (acetate) and exhibited increased flow through the tricarboxylic acid cycle and the glycolytic pathway. These three changes all lead to an increase in substrate level phosphorylation; the first two changes also lead to increased production of reducing equivalents. We interpret these data as indicating that E. coli makes use of its ability to respire even if it cannot directly couple this ability to ATP synthesis; by respiring away excess reducing equivalents E. coli enhances substrate level ATP synthesis.
    Original languageEnglish
    JournalJournal of Bacteriology
    Volume174
    Issue number23
    Pages (from-to)7635-7641
    Number of pages7
    ISSN0021-9193
    Publication statusPublished - 1992

    Keywords

    • Adenosine Diphosphate
    • Adenosine Triphosphate
    • Carbon
    • Citric Acid Cycle
    • Cytochrome b Group
    • Energy Metabolism
    • Escherichia coli
    • Gene Deletion
    • Glycolysis
    • Membrane Potentials
    • Oxidation-Reduction
    • Oxygen Consumption
    • Proton-Translocating ATPases
    • 61D2G4IYVH Adenosine Diphosphate
    • 7440-44-0 Carbon
    • 8L70Q75FXE Adenosine Triphosphate
    • EC 3.6.3.14 Proton-Translocating ATPases
    • ACETATE
    • ATP SYNTHESIS
    • GLYCOLYSIS
    • GROWTH RATE
    • GROWTH YIELD
    • MEMBRANE-BOUND PROTON TRANSLOCATING ATPASE
    • OXIDATIVE PHOSPHORYLATION
    • RESPIRATION
    • TRICARBOXYLIC ACID PATHWAY
    • TYPE B CYTOCHROMES
    • Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Escherichia coli
    • ACETATE 71-50-1
    • ATP 56-65-5Q, 42530-29-0Q, 94587-45-8Q, 111839-44-2Q
    • ATPASE 9000-83-3
    • CARBON 7440-44-0
    • 10060, Biochemistry studies - General
    • 10062, Biochemistry studies - Nucleic acids, purines and pyrimidines
    • 10064, Biochemistry studies - Proteins, peptides and amino acids
    • 10068, Biochemistry studies - Carbohydrates
    • 10508, Biophysics - Membrane phenomena
    • 10510, Biophysics - Bioenergetics: electron transport and oxidative phosphorylation
    • 10802, Enzymes - General and comparative studies: coenzymes
    • 10808, Enzymes - Physiological studies
    • 13002, Metabolism - General metabolism and metabolic pathways
    • 13003, Metabolism - Energy and respiratory metabolism
    • 13004, Metabolism - Carbohydrates
    • 13014, Metabolism - Nucleic acids, purines and pyrimidines
    • 25508, Development and Embryology - Morphogenesis
    • 31000, Physiology and biochemistry of bacteria
    • 31500, Genetics of bacteria and viruses
    • Biochemistry and Molecular Biophysics
    • Bioenergetics
    • Enzymology
    • Genetics
    • Metabolism
    • Physiology

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