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Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli


Sévin, Daniel C; Sauer, Uwe (2014). Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli. Nature Chemical Biology, 10(4):266-272.

Abstract

Bacteria are thought to cope with fluctuating environmental solute concentrations primarily by adjusting the osmolality of their cytoplasm. To obtain insights into underlying metabolic adaptions, we analyzed the global metabolic response of Escherichia coli to sustained hyperosmotic stress using non-targeted mass spectrometry. We observed that 52% of 1,071 detected metabolites, including known osmoprotectants, changed abundance with increasing salt challenge. Unexpectedly, unsupervised data analysis revealed a substantial increase of most intermediates in the ubiquinone-8 (Q8) biosynthesis pathway and a 110-fold accumulation of Q8 itself, as confirmed by quantitative lipidomics. We then demonstrate that Q8 is necessary for acute and sustained osmotic stress tolerance using Q8 mutants and tolerance rescue through feeding non-respiratory Q8 analogues. Finally, in vitro
experiments with artificial liposomes reveal mechanical membrane stabilization as a principal mechanism of Q8-mediated osmoprotection. Thus, we find that besides regulating intracellular osmolality, E. coli enhances its cytoplasmic membrane stability to withstand osmotic stress.

Abstract

Bacteria are thought to cope with fluctuating environmental solute concentrations primarily by adjusting the osmolality of their cytoplasm. To obtain insights into underlying metabolic adaptions, we analyzed the global metabolic response of Escherichia coli to sustained hyperosmotic stress using non-targeted mass spectrometry. We observed that 52% of 1,071 detected metabolites, including known osmoprotectants, changed abundance with increasing salt challenge. Unexpectedly, unsupervised data analysis revealed a substantial increase of most intermediates in the ubiquinone-8 (Q8) biosynthesis pathway and a 110-fold accumulation of Q8 itself, as confirmed by quantitative lipidomics. We then demonstrate that Q8 is necessary for acute and sustained osmotic stress tolerance using Q8 mutants and tolerance rescue through feeding non-respiratory Q8 analogues. Finally, in vitro
experiments with artificial liposomes reveal mechanical membrane stabilization as a principal mechanism of Q8-mediated osmoprotection. Thus, we find that besides regulating intracellular osmolality, E. coli enhances its cytoplasmic membrane stability to withstand osmotic stress.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:Special Collections > SystemsX.ch
Special Collections > SystemsX.ch > Research, Technology and Development Projects > MetaNetX
Special Collections > SystemsX.ch > Research, Technology and Development Projects
Dewey Decimal Classification:570 Life sciences; biology
Language:English
Date:February 2014
Deposited On:10 Feb 2014 14:22
Last Modified:05 Apr 2016 17:40
Publisher:Nature Publishing Group
ISSN:1552-4450
Publisher DOI:https://doi.org/10.1038/NCHEMBIO.1437
PubMed ID:24509820

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