Experimental determination of control by the H+-ATPase in Escherichia coli

Peter Ruhdal Jensen, Ole Michelsen, H. V. Westerhoff

    Research output: Contribution to journalJournal articleResearchpeer-review

    Abstract

    Strains carrying deletions in the atp genes, encoding the H+-ATPase, were unable to grow on nonfermentable substrates such as succinate, whereas with glucose as the substrate the growth rate of an atp deletion mutant was surprisingly high (some 75-80% of wild-type growth rate). The rate of glucose and oxygen consumption of these mutants was increased compared to the wild-type rates. In order to analyze the importance of the H+-ATPase at its physiological level, the cellular concentration of H+-ATPase was modulated around the wild-type level, using genetically manipulated strains. The control coefficient by the H+-ATPase with respect to growth rate and catabolic fluxes was measured. Control on growth rate was absent at the wildtype concentration of H+-ATPase, independent of whether the substrate for growth was glucose or succinate. Control by the H+-ATPase on the catabolic fluxes, including respiration, was negative at the wild-type H+-ATPase level. Moreover, the turnover number of the individual H+-ATPase enzymes increased as the H+-ATPase concentration was lowered. The negative control by the H+-ATPase on catabolism may thus be involved in a homeostatic control of ATP synthesis and, to some extent, explain the zero control by the H+-ATPase on E. coli growth rate.
    Original languageEnglish
    JournalJournal of Bioenergetics and Biomembranes
    Volume27
    Issue number6
    Pages (from-to)543-554
    Number of pages12
    ISSN0145-479X
    DOIs
    Publication statusPublished - 1995

    Keywords

    • Escherichia coli
    • Gene Deletion
    • Genes, Bacterial
    • Glucose
    • Kinetics
    • Operon
    • Oxygen Consumption
    • Proton-Translocating ATPases
    • Succinates
    • EC 3.6.3.14 Proton-Translocating ATPases
    • IY9XDZ35W2 Glucose
    • BIOPHYSICS
    • CELL
    • PROTON-TRANSLOCATING ATPASE
    • NUCLEOTIDE-SEQUENCE
    • OXIDATIVE-PHOSPHORYLATION
    • ADENOSINE-TRIPHOSPHATASE
    • SYNTHASE
    • OPERON
    • GENES
    • PROMOTERS
    • SUBUNIT
    • MUTATIONS
    • oxidative phosphorylation
    • respiration
    • ATP
    • fluxes
    • Metabolic Control Analysis
    • Oxidative phosphorylation
    • ATP GENE
    • BACTERIAL GROWTH RATE
    • CATABOLIC FLUX
    • GENETICS
    • MUTATION
    • OXIDATIVE PHOSPHORYLATION
    • OXYGEN CONSUMPTION
    • RESPIRATION
    • Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Escherichia coli
    • ATP 56-65-5Q, 42530-29-0Q, 94587-45-8Q, 111839-44-2Q
    • ATPASE 9000-83-3
    • OXYGEN 7782-44-7
    • 02506, Cytology - Animal
    • 10012, Biochemistry - Gases
    • 10060, Biochemistry studies - General
    • 10062, Biochemistry studies - Nucleic acids, purines and pyrimidines
    • 10510, Biophysics - Bioenergetics: electron transport and oxidative phosphorylation
    • 10808, Enzymes - Physiological studies
    • 13003, Metabolism - Energy and respiratory metabolism
    • 16004, Respiratory system - Physiology and biochemistry
    • 31000, Physiology and biochemistry of bacteria
    • 31500, Genetics of bacteria and viruses
    • 36002, Medical and clinical microbiology - Bacteriology
    • Biochemistry and Molecular Biophysics
    • Bioenergetics
    • Cell Biology
    • Enzymology
    • Genetics
    • Infection
    • Metabolism
    • Physiology

    Cite this

    @article{5f9abb92db7c43849c0dd945939950bb,
    title = "Experimental determination of control by the H+-ATPase in Escherichia coli",
    abstract = "Strains carrying deletions in the atp genes, encoding the H+-ATPase, were unable to grow on nonfermentable substrates such as succinate, whereas with glucose as the substrate the growth rate of an atp deletion mutant was surprisingly high (some 75-80{\%} of wild-type growth rate). The rate of glucose and oxygen consumption of these mutants was increased compared to the wild-type rates. In order to analyze the importance of the H+-ATPase at its physiological level, the cellular concentration of H+-ATPase was modulated around the wild-type level, using genetically manipulated strains. The control coefficient by the H+-ATPase with respect to growth rate and catabolic fluxes was measured. Control on growth rate was absent at the wildtype concentration of H+-ATPase, independent of whether the substrate for growth was glucose or succinate. Control by the H+-ATPase on the catabolic fluxes, including respiration, was negative at the wild-type H+-ATPase level. Moreover, the turnover number of the individual H+-ATPase enzymes increased as the H+-ATPase concentration was lowered. The negative control by the H+-ATPase on catabolism may thus be involved in a homeostatic control of ATP synthesis and, to some extent, explain the zero control by the H+-ATPase on E. coli growth rate.",
    keywords = "Escherichia coli, Gene Deletion, Genes, Bacterial, Glucose, Kinetics, Operon, Oxygen Consumption, Proton-Translocating ATPases, Succinates, EC 3.6.3.14 Proton-Translocating ATPases, IY9XDZ35W2 Glucose, BIOPHYSICS, CELL, PROTON-TRANSLOCATING ATPASE, NUCLEOTIDE-SEQUENCE, OXIDATIVE-PHOSPHORYLATION, ADENOSINE-TRIPHOSPHATASE, SYNTHASE, OPERON, GENES, PROMOTERS, SUBUNIT, MUTATIONS, oxidative phosphorylation, respiration, ATP, fluxes, Metabolic Control Analysis, Oxidative phosphorylation, ATP GENE, BACTERIAL GROWTH RATE, CATABOLIC FLUX, GENETICS, MUTATION, OXIDATIVE PHOSPHORYLATION, OXYGEN CONSUMPTION, RESPIRATION, Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Escherichia coli, ATP 56-65-5Q, 42530-29-0Q, 94587-45-8Q, 111839-44-2Q, ATPASE 9000-83-3, OXYGEN 7782-44-7, 02506, Cytology - Animal, 10012, Biochemistry - Gases, 10060, Biochemistry studies - General, 10062, Biochemistry studies - Nucleic acids, purines and pyrimidines, 10510, Biophysics - Bioenergetics: electron transport and oxidative phosphorylation, 10808, Enzymes - Physiological studies, 13003, Metabolism - Energy and respiratory metabolism, 16004, Respiratory system - Physiology and biochemistry, 31000, Physiology and biochemistry of bacteria, 31500, Genetics of bacteria and viruses, 36002, Medical and clinical microbiology - Bacteriology, Biochemistry and Molecular Biophysics, Bioenergetics, Cell Biology, Enzymology, Genetics, Infection, Metabolism, Physiology",
    author = "Jensen, {Peter Ruhdal} and Ole Michelsen and Westerhoff, {H. V.}",
    year = "1995",
    doi = "10.1007/BF02111653",
    language = "English",
    volume = "27",
    pages = "543--554",
    journal = "Journal of Bioenergetics and Biomembranes",
    issn = "0145-479X",
    publisher = "Springer",
    number = "6",

    }

    Experimental determination of control by the H+-ATPase in Escherichia coli. / Jensen, Peter Ruhdal; Michelsen, Ole; Westerhoff, H. V.

    In: Journal of Bioenergetics and Biomembranes, Vol. 27, No. 6, 1995, p. 543-554.

    Research output: Contribution to journalJournal articleResearchpeer-review

    TY - JOUR

    T1 - Experimental determination of control by the H+-ATPase in Escherichia coli

    AU - Jensen, Peter Ruhdal

    AU - Michelsen, Ole

    AU - Westerhoff, H. V.

    PY - 1995

    Y1 - 1995

    N2 - Strains carrying deletions in the atp genes, encoding the H+-ATPase, were unable to grow on nonfermentable substrates such as succinate, whereas with glucose as the substrate the growth rate of an atp deletion mutant was surprisingly high (some 75-80% of wild-type growth rate). The rate of glucose and oxygen consumption of these mutants was increased compared to the wild-type rates. In order to analyze the importance of the H+-ATPase at its physiological level, the cellular concentration of H+-ATPase was modulated around the wild-type level, using genetically manipulated strains. The control coefficient by the H+-ATPase with respect to growth rate and catabolic fluxes was measured. Control on growth rate was absent at the wildtype concentration of H+-ATPase, independent of whether the substrate for growth was glucose or succinate. Control by the H+-ATPase on the catabolic fluxes, including respiration, was negative at the wild-type H+-ATPase level. Moreover, the turnover number of the individual H+-ATPase enzymes increased as the H+-ATPase concentration was lowered. The negative control by the H+-ATPase on catabolism may thus be involved in a homeostatic control of ATP synthesis and, to some extent, explain the zero control by the H+-ATPase on E. coli growth rate.

    AB - Strains carrying deletions in the atp genes, encoding the H+-ATPase, were unable to grow on nonfermentable substrates such as succinate, whereas with glucose as the substrate the growth rate of an atp deletion mutant was surprisingly high (some 75-80% of wild-type growth rate). The rate of glucose and oxygen consumption of these mutants was increased compared to the wild-type rates. In order to analyze the importance of the H+-ATPase at its physiological level, the cellular concentration of H+-ATPase was modulated around the wild-type level, using genetically manipulated strains. The control coefficient by the H+-ATPase with respect to growth rate and catabolic fluxes was measured. Control on growth rate was absent at the wildtype concentration of H+-ATPase, independent of whether the substrate for growth was glucose or succinate. Control by the H+-ATPase on the catabolic fluxes, including respiration, was negative at the wild-type H+-ATPase level. Moreover, the turnover number of the individual H+-ATPase enzymes increased as the H+-ATPase concentration was lowered. The negative control by the H+-ATPase on catabolism may thus be involved in a homeostatic control of ATP synthesis and, to some extent, explain the zero control by the H+-ATPase on E. coli growth rate.

    KW - Escherichia coli

    KW - Gene Deletion

    KW - Genes, Bacterial

    KW - Glucose

    KW - Kinetics

    KW - Operon

    KW - Oxygen Consumption

    KW - Proton-Translocating ATPases

    KW - Succinates

    KW - EC 3.6.3.14 Proton-Translocating ATPases

    KW - IY9XDZ35W2 Glucose

    KW - BIOPHYSICS

    KW - CELL

    KW - PROTON-TRANSLOCATING ATPASE

    KW - NUCLEOTIDE-SEQUENCE

    KW - OXIDATIVE-PHOSPHORYLATION

    KW - ADENOSINE-TRIPHOSPHATASE

    KW - SYNTHASE

    KW - OPERON

    KW - GENES

    KW - PROMOTERS

    KW - SUBUNIT

    KW - MUTATIONS

    KW - oxidative phosphorylation

    KW - respiration

    KW - ATP

    KW - fluxes

    KW - Metabolic Control Analysis

    KW - Oxidative phosphorylation

    KW - ATP GENE

    KW - BACTERIAL GROWTH RATE

    KW - CATABOLIC FLUX

    KW - GENETICS

    KW - MUTATION

    KW - OXIDATIVE PHOSPHORYLATION

    KW - OXYGEN CONSUMPTION

    KW - RESPIRATION

    KW - Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Escherichia coli

    KW - ATP 56-65-5Q, 42530-29-0Q, 94587-45-8Q, 111839-44-2Q

    KW - ATPASE 9000-83-3

    KW - OXYGEN 7782-44-7

    KW - 02506, Cytology - Animal

    KW - 10012, Biochemistry - Gases

    KW - 10060, Biochemistry studies - General

    KW - 10062, Biochemistry studies - Nucleic acids, purines and pyrimidines

    KW - 10510, Biophysics - Bioenergetics: electron transport and oxidative phosphorylation

    KW - 10808, Enzymes - Physiological studies

    KW - 13003, Metabolism - Energy and respiratory metabolism

    KW - 16004, Respiratory system - Physiology and biochemistry

    KW - 31000, Physiology and biochemistry of bacteria

    KW - 31500, Genetics of bacteria and viruses

    KW - 36002, Medical and clinical microbiology - Bacteriology

    KW - Biochemistry and Molecular Biophysics

    KW - Bioenergetics

    KW - Cell Biology

    KW - Enzymology

    KW - Genetics

    KW - Infection

    KW - Metabolism

    KW - Physiology

    U2 - 10.1007/BF02111653

    DO - 10.1007/BF02111653

    M3 - Journal article

    VL - 27

    SP - 543

    EP - 554

    JO - Journal of Bioenergetics and Biomembranes

    JF - Journal of Bioenergetics and Biomembranes

    SN - 0145-479X

    IS - 6

    ER -