A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis

Abstract The transition between the planktonic state and the biofilm-associated state is a key developmental decision for pathogenic bacteria. Biofilm formation by Yersinia pestis is regulated by hmsHFRS genes (β-1, 6-N-acetyl-D-glucosamine synthesis operon) in its flea vector and in vitro. However,...

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Main Authors: Ruoxi Zhao, Yunhong Song, Qingyun Dai, Yiwen Kang, Junfeng Pan, Lingfang Zhu, Lei Zhang, Yao Wang, Xihui Shen
Format: Article
Language:English
Published: Nature Publishing Group 2017-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-00534-9
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spelling doaj-36c8f1925d7b4508bf071a77cfd54d332020-12-08T02:48:28ZengNature Publishing GroupScientific Reports2045-23222017-04-017111310.1038/s41598-017-00534-9A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosisRuoxi Zhao0Yunhong Song1Qingyun Dai2Yiwen Kang3Junfeng Pan4Lingfang Zhu5Lei Zhang6Yao Wang7Xihui Shen8State Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityState Key Laboratory of Crop Stress Biology for Arid Areas and College of Life Sciences, Northwest A&F UniversityAbstract The transition between the planktonic state and the biofilm-associated state is a key developmental decision for pathogenic bacteria. Biofilm formation by Yersinia pestis is regulated by hmsHFRS genes (β-1, 6-N-acetyl-D-glucosamine synthesis operon) in its flea vector and in vitro. However, the mechanism of biofilm formation in Yersinia pseudotuberculosis remains elusive. In this study, we demonstrate that the LysR-type regulator RovM inversely regulates biofilm formation and motility in Y. pseudotuberculosis by acting as a transcriptional regulator of these two functions. RovM is strongly induced during growth in minimal media but strongly repressed in complex media. On one hand, RovM enhances bacterial motility by activating the expression of FlhDC, the master regulator of flagellar genes, via the recognition of an operator upstream of the flhDC promoter. On the other hand, RovM represses β-GlcNAc production under nutrition-limited conditions, negatively regulating hmsHFRS expression by directly binding to the −35 element of its promoter. Compared to wild-type bacteria, the rovM mutant established denser biofilms and caused more extensive mortality in mice and silkworm larvae. These results indicate that RovM acts as a molecular switch to coordinate the expression of genes involved in biofilm formation and motility in response to the availability of nutrients.https://doi.org/10.1038/s41598-017-00534-9
collection DOAJ
language English
format Article
sources DOAJ
author Ruoxi Zhao
Yunhong Song
Qingyun Dai
Yiwen Kang
Junfeng Pan
Lingfang Zhu
Lei Zhang
Yao Wang
Xihui Shen
spellingShingle Ruoxi Zhao
Yunhong Song
Qingyun Dai
Yiwen Kang
Junfeng Pan
Lingfang Zhu
Lei Zhang
Yao Wang
Xihui Shen
A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis
Scientific Reports
author_facet Ruoxi Zhao
Yunhong Song
Qingyun Dai
Yiwen Kang
Junfeng Pan
Lingfang Zhu
Lei Zhang
Yao Wang
Xihui Shen
author_sort Ruoxi Zhao
title A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis
title_short A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis
title_full A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis
title_fullStr A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis
title_full_unstemmed A starvation-induced regulator, RovM, acts as a switch for planktonic/biofilm state transition in Yersinia pseudotuberculosis
title_sort starvation-induced regulator, rovm, acts as a switch for planktonic/biofilm state transition in yersinia pseudotuberculosis
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-04-01
description Abstract The transition between the planktonic state and the biofilm-associated state is a key developmental decision for pathogenic bacteria. Biofilm formation by Yersinia pestis is regulated by hmsHFRS genes (β-1, 6-N-acetyl-D-glucosamine synthesis operon) in its flea vector and in vitro. However, the mechanism of biofilm formation in Yersinia pseudotuberculosis remains elusive. In this study, we demonstrate that the LysR-type regulator RovM inversely regulates biofilm formation and motility in Y. pseudotuberculosis by acting as a transcriptional regulator of these two functions. RovM is strongly induced during growth in minimal media but strongly repressed in complex media. On one hand, RovM enhances bacterial motility by activating the expression of FlhDC, the master regulator of flagellar genes, via the recognition of an operator upstream of the flhDC promoter. On the other hand, RovM represses β-GlcNAc production under nutrition-limited conditions, negatively regulating hmsHFRS expression by directly binding to the −35 element of its promoter. Compared to wild-type bacteria, the rovM mutant established denser biofilms and caused more extensive mortality in mice and silkworm larvae. These results indicate that RovM acts as a molecular switch to coordinate the expression of genes involved in biofilm formation and motility in response to the availability of nutrients.
url https://doi.org/10.1038/s41598-017-00534-9
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