Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.

An important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we com...

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Main Authors: Stuart D Woodcock, Karl Syson, Richard H Little, Danny Ward, Despoina Sifouna, James K M Brown, Stephen Bornemann, Jacob G Malone
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-04-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009524&type=printable
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author Stuart D Woodcock
Karl Syson
Richard H Little
Danny Ward
Despoina Sifouna
James K M Brown
Stephen Bornemann
Jacob G Malone
author_facet Stuart D Woodcock
Karl Syson
Richard H Little
Danny Ward
Despoina Sifouna
James K M Brown
Stephen Bornemann
Jacob G Malone
author_sort Stuart D Woodcock
collection DOAJ
description An important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we combine molecular biology and biochemistry to dissect the trehalose metabolic network in the opportunistic human pathogen Pseudomonas aeruginosa PAO1 and define its role in abiotic stress protection. We show that trehalose metabolism in PAO1 is integrated with the biosynthesis of branched α-glucan (glycogen), with mutants in either biosynthetic pathway significantly compromised for survival on abiotic surfaces. While both trehalose and α-glucan are important for abiotic stress tolerance, we show they counter distinct stresses. Trehalose is important for the PAO1 osmotic stress response, with trehalose synthesis mutants displaying severely compromised growth in elevated salt conditions. However, trehalose does not contribute directly to the PAO1 desiccation response. Rather, desiccation tolerance is mediated directly by GlgE-derived α-glucan, with deletion of the glgE synthase gene compromising PAO1 survival in low humidity but having little effect on osmotic sensitivity. Desiccation tolerance is independent of trehalose concentration, marking a clear distinction between the roles of these two molecules in mediating responses to abiotic stress.
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spelling doaj-art-58fb014f6826408c94589a6c9edfcbb62025-08-20T02:33:43ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-04-01174e100952410.1371/journal.pgen.1009524Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.Stuart D WoodcockKarl SysonRichard H LittleDanny WardDespoina SifounaJames K M BrownStephen BornemannJacob G MaloneAn important prelude to bacterial infection is the ability of a pathogen to survive independently of the host and to withstand environmental stress. The compatible solute trehalose has previously been connected with diverse abiotic stress tolerances, particularly osmotic shock. In this study, we combine molecular biology and biochemistry to dissect the trehalose metabolic network in the opportunistic human pathogen Pseudomonas aeruginosa PAO1 and define its role in abiotic stress protection. We show that trehalose metabolism in PAO1 is integrated with the biosynthesis of branched α-glucan (glycogen), with mutants in either biosynthetic pathway significantly compromised for survival on abiotic surfaces. While both trehalose and α-glucan are important for abiotic stress tolerance, we show they counter distinct stresses. Trehalose is important for the PAO1 osmotic stress response, with trehalose synthesis mutants displaying severely compromised growth in elevated salt conditions. However, trehalose does not contribute directly to the PAO1 desiccation response. Rather, desiccation tolerance is mediated directly by GlgE-derived α-glucan, with deletion of the glgE synthase gene compromising PAO1 survival in low humidity but having little effect on osmotic sensitivity. Desiccation tolerance is independent of trehalose concentration, marking a clear distinction between the roles of these two molecules in mediating responses to abiotic stress.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009524&type=printable
spellingShingle Stuart D Woodcock
Karl Syson
Richard H Little
Danny Ward
Despoina Sifouna
James K M Brown
Stephen Bornemann
Jacob G Malone
Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.
PLoS Genetics
title Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.
title_full Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.
title_fullStr Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.
title_full_unstemmed Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.
title_short Trehalose and α-glucan mediate distinct abiotic stress responses in Pseudomonas aeruginosa.
title_sort trehalose and α glucan mediate distinct abiotic stress responses in pseudomonas aeruginosa
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1009524&type=printable
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