Respiratory Control in <i>Escherichia coli</i> K 12

Burstein, Claude; Tiankova, Lina; Képès, Adam

doi:10.1111/j.1432-1033.1979.tb12905.x

Cited by 47 publications

(32 citation statements)

References 18 publications

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“…This might explain why it has been impossible to show an increase in the respiration rate of exponentially growing E. coli cells after addition of an uncoupler (respiratory control) (2,23).…”

Section: Discussionmentioning

confidence: 99%

Carbon and energy metabolism of atp mutants of Escherichia coli

1992

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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%o, 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%o 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. colh 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.The membrane-bound ATP synthase of Escherichia coli has a central role in free-energy transduction under aerobic and anaerobic growth conditions. Under aerobic conditions, the proton motive force generated by the respiratory chain is utilized by the ATP synthase to drive ATP synthesis and to maintain solute gradients. Under anaerobic conditions, the proton motive force can be generated by the ATP synthase through hydrolysis of ATP. The atp operon, which encodes the ATP synthase, consists of nine genes in the following order: atpIBEFHAGDC (12,19,20). atpI encodes a 14-kDa protein of unknown function and has been shown to be dispensable (28). atpBEF encodes the three subunits that form the membrane-integrated Fo part (the proton channel), whereas atpHAGDC encodes the five subunits that form the cytoplasmic F, part (the ATPase) (12,20).von Meyenburg et al. (27) analyzed the growth of strains that lack an intact ATP synthase. These strains are not able to grow on nonfermentative carbon sources, such as acetate or succinate. The growth rate and growth yield in aerobic minimal glucose medium were reduced to 75 and 55% of the wild-type levels, respectively. Mutant strains with Tn1O insertions in the promoter region of the atp operon also exhibited a reduced growth yield that ...

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Section: Discussionmentioning

confidence: 99%

Carbon and energy metabolism of atp mutants of Escherichia coli

1992

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“…Previous bioenergetic experiments with respiring E. coli and mitochondria have shown that the membrane potential and the rate of respiration are inversely related (5,28). In a regulatory loop known as respiratory control, increases in the membrane potential slow processes that transport protons out of the cell by increasing the energy required to pump protons across the membrane.…”

Section: ϫ2mentioning

confidence: 99%

Enhancement of Survival and Electricity Production in an Engineered Bacterium by Light-Driven Proton Pumping

Johnson

Baron

Naranjo

et al. 2010

Appl Environ Microbiol

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Microorganisms can use complex photosystems or light-dependent proton pumps to generate membrane potential and/or reduce electron carriers to support growth. The discovery that proteorhodopsin is a light-dependent proton pump that can be expressed readily in recombinant bacteria enables development of new strategies to probe microbial physiology and to engineer microbes with new light-driven properties. Here, we describe functional expression of proteorhodopsin and light-induced changes in membrane potential in the bacterium Shewanella oneidensis strain MR-1. We report that there were significant increases in electrical current generation during illumination of electrochemical chambers containing S. oneidensis expressing proteorhodopsin. We present evidence that an engineered strain is able to consume lactate at an increased rate when it is illuminated, which is consistent with the hypothesis that proteorhodopsin activity enhances lactate uptake by increasing the proton motive force. Our results demonstrate that there is coupling of a light-driven process to electricity generation in a nonphotosynthetic engineered bacterium. Expression of proteorhodopsin also preserved the viability of the bacterium under nutrient-limited conditions, providing evidence that fulfillment of basic energy needs of organisms may explain the widespread distribution of proteorhodopsin in marine environments.

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“…In contrast to CDI, cells recovering growth in the presence of CCCP do not appear to recover ⌬p, leading Kinoshita and coworkers to conclude that E. coli can grow in the absence of ⌬p after a lag period (35) during which the bacteria presumably alter gene expression to adapt to uncoupler (23). Addition of CCCP causes an increase in respiration in starved E. coli, the opposite response to that we observe in CDI (15,40). Thus, it seems unlikely that the mechanism of CDI involves solely a reduction in ⌬p, although this may contribute to growth inhibition.…”

Section: Discussionmentioning

confidence: 53%

“…Notably, respiration was repressed cotemporally with ⌬p and ATP (Fig. 4), the opposite of what has been observed to occur in mitochondria and starved bacteria exposed to uncoupling agents that dissipate ⌬p, such as CCCP (15,31). In the case of starved bacteria, respiratory control is lost, and cellular respiration is constitutively increased.…”

Section: Discussionmentioning

confidence: 77%

“…Mitochondria respond to a reduction in ⌬p by increasing respiration, a process involving respiratory control in which the ⌬p regulates electron transport, maintaining a constant ATP/ ADP ratio (13,14). In contrast, E. coli shows respiratory control under conditions of starvation only (15,40), possibly because under normal laboratory conditions, the rate of respiration is near maximal. The measurement of oxygen consumption indicated that respiration was significantly reduced in CDI ϩ cells cotemporally with growth inhibition, whereas respiration in CDI Ϫ control and CDI ϩ acrB mutant cells increased until a steady state was reached at about 3 h (Fig.…”

Section: Vol 191 2009 Cdi-induced Reversible Metabolic Downregulatimentioning

confidence: 99%

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Contact-Dependent Growth Inhibition Causes Reversible Metabolic Downregulation in Escherichia coli

et al. 2009

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Contact-dependent growth inhibition (CDI) is a mechanism identified in Escherichia coli by which bacteria expressing two-partner secretion proteins encoded by cdiA and cdiB bind to BamA in the outer membranes of target cells and inhibit their growth. A third gene in the cluster, cdiI, encodes a small protein that is necessary and sufficient to confer immunity to CDI, thereby preventing cells expressing the cdiBA genes from inhibiting their own growth. In this study, the cdiI gene was placed under araBAD promoter control to modulate levels of the immunity protein and thereby induce CDI by removal of arabinose. This CDI autoinhibition system was used for metabolic analyses of a single population of E. coli cells undergoing CDI. Contact-inhibited cells showed altered cell morphology, including the presence of filaments. Notably, CDI was reversible, as evidenced by resumption of cell growth and normal cellular morphology following induction of the CdiI immunity protein.Recovery of cells from CDI also required an energy source. Cells undergoing CDI showed a significant, reversible downregulation of metabolic parameters, including aerobic respiration, proton motive force (⌬p), and steady-state ATP levels. It is unclear whether the decrease in respiration and/or ⌬p is directly involved in growth inhibition, but a role for ATP in the CDI mechanism was ruled out using an atp mutant. Consistent with the observed decrease in ⌬p, the phage shock response was induced in cells undergoing CDI but not in recovering cells, based on analysis of levels of pspA mRNA.

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Respiratory Control in Escherichia coli K 12

Cited by 47 publications

References 18 publications

Carbon and energy metabolism of atp mutants of Escherichia coli

Carbon and energy metabolism of atp mutants of Escherichia coli

Enhancement of Survival and Electricity Production in an Engineered Bacterium by Light-Driven Proton Pumping

Contact-Dependent Growth Inhibition Causes Reversible Metabolic Downregulation in Escherichia coli

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