Elongation factor Tu: a molecular switch in protein biosynthesis

Weijland, Albert; Harmark, Kim; Cool, Robbert H.; Anborgh, Pieter H.; Parmeggiani, Andrea

doi:10.1111/j.1365-2958.1992.tb01516.x

Cited by 77 publications

(48 citation statements)

References 55 publications

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“…tufA is one of two unlinked genes (with tufB) coding for the translation elongation factor Tu, which promotes GTP-dependent binding of aminoacyltRNA to the A site of ribosomes during protein synthesis. Like sspA, tufA may play an important regulatory role in the bacterial response to nutrient deprivation (57,59).…”

Section: Resultsmentioning

confidence: 99%

The Amino Acid Valine Is Secreted in Continuous-Flow Bacterial Biofilms

Valle

Schmid

et al. 2008

J Bacteriol

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Biofilms are structured communities characterized by distinctive gene expression patterns and profound physiological changes compared to those of planktonic cultures. Here, we show that many gram-negative bacterial biofilms secrete high levels of a small-molecular-weight compound, which inhibits the growth of only Escherichia coli K-12 and a rare few other natural isolates. We demonstrate both genetically and biochemically that this molecule is the amino acid valine, and we provide evidence that valine production within biofilms results from metabolic changes occurring within high-density biofilm communities when carbon sources are not limiting. This finding identifies a natural environment in which bacteria can encounter high amounts of valine, and we propose that in-biofilm valine secretion may be the long-sought reason for widespread but unexplained valine resistance found in most enterobacteria. Our results experimentally validate the postulated production of metabolites that is characteristic of the conditions associated with some biofilm environments. The identification of such molecules may lead to new approaches for biofilm monitoring and control.Biofilms are matrix-encased bacterial communities that develop on most surfaces and often constitute a reservoir of bacterial pathogens. Detrimental biofilms are difficult to eradicate due to a characteristic tolerance to biocides. They cause serious health and economic problems when they form on medical and industrial devices (11,19,24). While biofilmassociated antibiotic tolerance is considered a major physiological trait that distinguishes free cells from surface-attached cells, biofilms are also characterized by gene expression patterns that are distinctive compared to those of planktonic cultures (4,35,40,41,58). These changes are likely to result from modifications of growth conditions within biofilms, and they have been proposed to correspond to ill-understood responses triggered by the biofilm lifestyle (3,26).Recently, studies conducted with simplified, mixed communities composed of two bacterial species revealed that biofilm bacteria express competitive or cooperative behavior that does not take place within classical planktonic cultures (7,22). These results suggested that biofilm-associated weaponry could contribute to the dynamics of bacterial biofilm populations. However, thus far, the production of molecules involved in antagonistic bacterial relationships within biofilms has been poorly investigated.Here we show that the continuous-flow biofilms formed by many Escherichia coli strains and other gram-negative bacteria accumulate high levels of a small-molecular-weight compound with inhibitory activity against E. coli K-12 strains. We demonstrate both genetically and biochemically that this compound is the amino acid valine. We provide evidence that valine secretion within biofilms could be the cause of the longknown but unexplained widespread valine resistance observed for most enterobacteria. Beyond the biological significance of in-biofilm valin...

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Section: Resultsmentioning

confidence: 99%

The Amino Acid Valine Is Secreted in Continuous-Flow Bacterial Biofilms

Valle

Schmid

et al. 2008

J Bacteriol

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“…In E. coli, exposure to cis-DA led to de novo production of proteins involved in transport (OppA), protein translation (TufA), metabolism (PoxB, FbaA, GadA, and SerC), and ATP synthesis and ATP hydrolysis (AtpA) (74)(75)(76)(77)(78)(79)(80). Proteins identified in E. coli under both cis-DA and saline conditions were involved in several functions, including metabolism (pyruvate dehydrogenase, AceF, and FrdA), ATP hydrolysis (polyphosphate kinase [PPK]), and protein repair (GroL) (81)(82)(83)(84)(85).…”

Section: Figmentioning

confidence: 99%

The Fatty Acid Signaling Molecule cis -2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State

Marques

Morozov

Planzos

et al. 2014

Appl Environ Microbiol

125

112

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bPersister cells, which are tolerant to antimicrobials, contribute to biofilm recalcitrance to therapeutic agents. In turn, the ability to kill persister cells is believed to significantly improve efforts in eradicating biofilm-related, chronic infections. While much research has focused on elucidating the mechanism(s) by which persister cells form, little is known about the mechanism or factors that enable persister cells to revert to an active and susceptible state. Here, we demonstrate that cis-2-decenoic acid (cis-DA), a fatty acid signaling molecule, is able to change the status of Pseudomonas aeruginosa and Escherichia coli persister cells from a dormant to a metabolically active state without an increase in cell number. This cell awakening is supported by an increase of the persister cells' respiratory activity together with changes in protein abundance and increases of the transcript expression levels of several metabolic markers, including acpP, 16S rRNA, atpH, and ppx. Given that most antimicrobials target actively growing cells, we also explored the effect of cis-DA on enhancing antibiotic efficacy in killing persister cells due to their inability to keep a persister cell state. Compared to antimicrobial treatment alone, combinational treatments of persister cell subpopulations with antimicrobials and cis-DA resulted in a significantly greater decrease in cell viability. In addition, the presence of cis-DA led to a decrease in the number of persister cells isolated. We thus demonstrate the ability of a fatty acid signaling molecule to revert bacterial cells from a tolerant phenotype to a metabolically active, antimicrobial-sensitive state. P ersister cells are considered to be a subpopulation of stochastically produced, nongrowing (dormant) cells present in biofilm and planktonic bacterial cultures. Persister cells account for 10 Ϫ6 to 10 Ϫ4 of the total cell population of mid-exponential-phase cells and up to 1% of the total cell population of stationary-phase cells and biofilms, a pattern resembling that of a quorum-sensing mechanism (1-3). Tolerance to antimicrobials is one of the key characteristics of this subpopulation, as persisters escape killing by antimicrobials such as fluoroquinolones, which can kill slowgrowing bacteria but not dormant cells (4). It is therefore not surprising that persister cells are considered to play a major role in the resilience of bacterial populations and have recently been isolated from patients with candidiasis, from cystic fibrosis patients with chronic lung infections, and from Mycobacterium tuberculosis biofilms responsible for chronic tuberculosis (5-8).Several mechanisms have been described to contribute to persister cell formation. For instance, several genes involved in energy generation and cell maintenance have been shown to be downregulated in persister cells, further indicating that persisters are nongrowing, dormant cells (1). Among these genes were members of several operons involved in oxidative phosphorylation, including NADH dehydrogenase, ATP syn...

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“…Of those with a known function, yfiA (translational stimulator ; Bylund et al, 1997), tufA\tufB (EF-Tu ; reviewed by Weijland et al, 1992) and yjbC (putative pseudouridylate synthase, shows similarity to rsuA ; Wrzesinski et al, 1995) encode proteins involved in translation ; this adaptation may comprise a general response to stress or may merely be a function of lower growth rates in the presence of a toxic agent. In addition, tnaA (tryptophanase ; Deeley & Yanofsky, 1981) and aspA (aspartase ; Guest et al, 1984) are reduced, suggesting the cell is less catabolic in nature.…”

Section: Transcriptional Analysis Of Adapted Strainsmentioning

confidence: 99%

Metal-ion tolerance in Escherichia coli: analysis of transcriptional profiles by gene-array technology

Brocklehurst

Morby

2000

Microbiology

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Escherichia coli was adapted to grow in medium containing substantially elevated concentrations of either Zn(II), Cd(II), Co(II) or Ni(II). Whole-genome transcriptional profiles were generated from adapted strains and analysed for significant alteration in transcript abundance with reference to a wild-type strain. Similar alterations in specific message levels were observed for strains adapted to the four metal ions. One unexpected trend was the increase in transcript level of genes involved in transposition of IS elements, particularly insA. Subsequent expression of insA-7 from a heterologous promoter in E. coli conferred tolerance to Zn(II).

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Elongation factor Tu: a molecular switch in protein biosynthesis

Cited by 77 publications

References 55 publications

The Amino Acid Valine Is Secreted in Continuous-Flow Bacterial Biofilms

The Amino Acid Valine Is Secreted in Continuous-Flow Bacterial Biofilms

The Fatty Acid Signaling Molecule cis -2-Decenoic Acid Increases Metabolic Activity and Reverts Persister Cells to an Antimicrobial-Susceptible State

Metal-ion tolerance in Escherichia coli: analysis of transcriptional profiles by gene-array technology

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