Activators of the glutamate-dependent acid resistance system alleviate deleterious effects of YidC depletion in Escherichia coli

Z. Yu, M. Bekker, A. Tramonti, G.M. Cook, P. van Ulsen, D.J. Scheffers, J.T. De Mattos, D. De Biase, J. Luirink

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

The function of the essential inner membrane protein (IMP) YidC in Escherichia coli has been studied for a limited number of model IMPs and primarily using targeted approaches. These studies suggested that YidC acts at the level of insertion, folding, and quality control of IMPs, both in the context of the Sec translocon and as a separate entity. To further our understanding of YidC's role in IMP biogenesis, we screened a random overexpression library for factors that rescued the growth of cells upon YidC depletion. We found that the overexpression of the GadX and GadY regulators of the glutamate-dependent acid resistance system complemented the growth defect of YidC-depleted cells. Evidence is presented that GadXY overexpression counteracts the deleterious effects of YidC depletion on at least two fronts. First, GadXY prepares the cells for the decrease in respiratory capacity upon the depletion of YidC. Most likely, GadXY-regulated processes reduce the drop in proton-motive force that impairs the fitness of YidC-depleted cells. Second, in GadXY-overproducing cells increased levels of the general chaperone GroEL cofractionate with the inner membranes, which may help to keep newly synthesized inner membrane proteins in an insertion-competent state when YidC levels are limiting. Copyright © 2011, American Society for Microbiology. All Rights Reserved.
LanguageEnglish
Pages1308-16
JournalJournal of Bacteriology
Volume193
DOIs
Publication statusPublished - 2011

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Glutamic Acid
Escherichia coli
Acids
Inosine Monophosphate
Membrane Proteins
Proton-Motive Force
Quality Control
Libraries
Intercellular Signaling Peptides and Proteins
Membranes
Growth

Bibliographical note

1098-5530 Yu, Zhong Bekker, Martijn Tramonti, Angela Cook, Gregory M van Ulsen, Peter Scheffers, Dirk-Jan de Mattos, Joost Teixeira De Biase, Daniela Luirink, Joen Journal Article United States J Bacteriol. 2011 Mar;193(6):1308-16. doi: 10.1128/JB.01209-10. Epub 2011 Jan 7.

Cite this

Yu, Z. ; Bekker, M. ; Tramonti, A. ; Cook, G.M. ; van Ulsen, P. ; Scheffers, D.J. ; De Mattos, J.T. ; De Biase, D. ; Luirink, J. / Activators of the glutamate-dependent acid resistance system alleviate deleterious effects of YidC depletion in Escherichia coli. In: Journal of Bacteriology. 2011 ; Vol. 193. pp. 1308-16.
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abstract = "The function of the essential inner membrane protein (IMP) YidC in Escherichia coli has been studied for a limited number of model IMPs and primarily using targeted approaches. These studies suggested that YidC acts at the level of insertion, folding, and quality control of IMPs, both in the context of the Sec translocon and as a separate entity. To further our understanding of YidC's role in IMP biogenesis, we screened a random overexpression library for factors that rescued the growth of cells upon YidC depletion. We found that the overexpression of the GadX and GadY regulators of the glutamate-dependent acid resistance system complemented the growth defect of YidC-depleted cells. Evidence is presented that GadXY overexpression counteracts the deleterious effects of YidC depletion on at least two fronts. First, GadXY prepares the cells for the decrease in respiratory capacity upon the depletion of YidC. Most likely, GadXY-regulated processes reduce the drop in proton-motive force that impairs the fitness of YidC-depleted cells. Second, in GadXY-overproducing cells increased levels of the general chaperone GroEL cofractionate with the inner membranes, which may help to keep newly synthesized inner membrane proteins in an insertion-competent state when YidC levels are limiting. Copyright {\circledC} 2011, American Society for Microbiology. All Rights Reserved.",
author = "Z. Yu and M. Bekker and A. Tramonti and G.M. Cook and {van Ulsen}, P. and D.J. Scheffers and {De Mattos}, J.T. and {De Biase}, D. and J. Luirink",
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Activators of the glutamate-dependent acid resistance system alleviate deleterious effects of YidC depletion in Escherichia coli. / Yu, Z.; Bekker, M.; Tramonti, A.; Cook, G.M.; van Ulsen, P.; Scheffers, D.J.; De Mattos, J.T.; De Biase, D.; Luirink, J.

In: Journal of Bacteriology, Vol. 193, 2011, p. 1308-16.

Research output: Contribution to JournalArticleAcademicpeer-review

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T1 - Activators of the glutamate-dependent acid resistance system alleviate deleterious effects of YidC depletion in Escherichia coli

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AU - Bekker, M.

AU - Tramonti, A.

AU - Cook, G.M.

AU - van Ulsen, P.

AU - Scheffers, D.J.

AU - De Mattos, J.T.

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N2 - The function of the essential inner membrane protein (IMP) YidC in Escherichia coli has been studied for a limited number of model IMPs and primarily using targeted approaches. These studies suggested that YidC acts at the level of insertion, folding, and quality control of IMPs, both in the context of the Sec translocon and as a separate entity. To further our understanding of YidC's role in IMP biogenesis, we screened a random overexpression library for factors that rescued the growth of cells upon YidC depletion. We found that the overexpression of the GadX and GadY regulators of the glutamate-dependent acid resistance system complemented the growth defect of YidC-depleted cells. Evidence is presented that GadXY overexpression counteracts the deleterious effects of YidC depletion on at least two fronts. First, GadXY prepares the cells for the decrease in respiratory capacity upon the depletion of YidC. Most likely, GadXY-regulated processes reduce the drop in proton-motive force that impairs the fitness of YidC-depleted cells. Second, in GadXY-overproducing cells increased levels of the general chaperone GroEL cofractionate with the inner membranes, which may help to keep newly synthesized inner membrane proteins in an insertion-competent state when YidC levels are limiting. Copyright © 2011, American Society for Microbiology. All Rights Reserved.

AB - The function of the essential inner membrane protein (IMP) YidC in Escherichia coli has been studied for a limited number of model IMPs and primarily using targeted approaches. These studies suggested that YidC acts at the level of insertion, folding, and quality control of IMPs, both in the context of the Sec translocon and as a separate entity. To further our understanding of YidC's role in IMP biogenesis, we screened a random overexpression library for factors that rescued the growth of cells upon YidC depletion. We found that the overexpression of the GadX and GadY regulators of the glutamate-dependent acid resistance system complemented the growth defect of YidC-depleted cells. Evidence is presented that GadXY overexpression counteracts the deleterious effects of YidC depletion on at least two fronts. First, GadXY prepares the cells for the decrease in respiratory capacity upon the depletion of YidC. Most likely, GadXY-regulated processes reduce the drop in proton-motive force that impairs the fitness of YidC-depleted cells. Second, in GadXY-overproducing cells increased levels of the general chaperone GroEL cofractionate with the inner membranes, which may help to keep newly synthesized inner membrane proteins in an insertion-competent state when YidC levels are limiting. Copyright © 2011, American Society for Microbiology. All Rights Reserved.

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