Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli

Abstract Stochastic switching is considered as a cost‐saving strategy for adaptation to environmental challenges. We show here that stochastic switching of a monostable circuit can mediate the adaptation of the engineered OSU12‐hisC Escherichia coli strain to histidine starvation. In this strain, th...

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Main Authors: Saburo Tsuru, Nao Yasuda, Yoshie Murakami, Junya Ushioda, Akiko Kashiwagi, Shingo Suzuki, Kotaro Mori, Bei‐Wen Ying, Tetsuya Yomo
Format: Article
Language:English
Published: Springer Nature 2011-05-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.1038/msb.2011.24
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author Saburo Tsuru
Nao Yasuda
Yoshie Murakami
Junya Ushioda
Akiko Kashiwagi
Shingo Suzuki
Kotaro Mori
Bei‐Wen Ying
Tetsuya Yomo
author_facet Saburo Tsuru
Nao Yasuda
Yoshie Murakami
Junya Ushioda
Akiko Kashiwagi
Shingo Suzuki
Kotaro Mori
Bei‐Wen Ying
Tetsuya Yomo
author_sort Saburo Tsuru
collection DOAJ
description Abstract Stochastic switching is considered as a cost‐saving strategy for adaptation to environmental challenges. We show here that stochastic switching of a monostable circuit can mediate the adaptation of the engineered OSU12‐hisC Escherichia coli strain to histidine starvation. In this strain, the hisC gene was deleted from the His operon and placed under the control of a monostable foreign promoter. In response to histidine depletion, the OSU12‐hisC population shifted to a higher HisC expression level, which is beneficial under starving conditions but is not favoured by the monostable circuit. The population shift was accompanied by growth recovery and was reversible upon histidine addition. A weak directionality in stochastic switching of hisC was observed in growing microcolonies under histidine‐free conditions. Directionality and fate decision were in part dependent on the initial cellular status. Finally, microarray analysis indicated that OSU12‐hisC reorganized its transcriptome to reach the appropriate physiological state upon starvation. These findings suggest that bacteria do not necessarily need to evolve signalling mechanisms to control gene expression appropriately, even for essential genes.
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publisher Springer Nature
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series Molecular Systems Biology
spelling doaj-art-45e52bda478c4a5ea4ae1808463770672025-08-20T02:11:49ZengSpringer NatureMolecular Systems Biology1744-42922011-05-017111010.1038/msb.2011.24Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coliSaburo Tsuru0Nao Yasuda1Yoshie Murakami2Junya Ushioda3Akiko Kashiwagi4Shingo Suzuki5Kotaro Mori6Bei‐Wen Ying7Tetsuya Yomo8Department of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka UniversityGraduate School of Frontier Biosciences, Osaka UniversityDepartment of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka UniversityDepartment of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka UniversityFaculty of Agriculture and Life Science, Hirosaki UniversityDepartment of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka UniversityGraduate School of Frontier Biosciences, Osaka UniversityDepartment of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka UniversityDepartment of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka UniversityAbstract Stochastic switching is considered as a cost‐saving strategy for adaptation to environmental challenges. We show here that stochastic switching of a monostable circuit can mediate the adaptation of the engineered OSU12‐hisC Escherichia coli strain to histidine starvation. In this strain, the hisC gene was deleted from the His operon and placed under the control of a monostable foreign promoter. In response to histidine depletion, the OSU12‐hisC population shifted to a higher HisC expression level, which is beneficial under starving conditions but is not favoured by the monostable circuit. The population shift was accompanied by growth recovery and was reversible upon histidine addition. A weak directionality in stochastic switching of hisC was observed in growing microcolonies under histidine‐free conditions. Directionality and fate decision were in part dependent on the initial cellular status. Finally, microarray analysis indicated that OSU12‐hisC reorganized its transcriptome to reach the appropriate physiological state upon starvation. These findings suggest that bacteria do not necessarily need to evolve signalling mechanisms to control gene expression appropriately, even for essential genes.https://doi.org/10.1038/msb.2011.24adaptationgene regulationmonostabilitystochastic switchingtransciptome
spellingShingle Saburo Tsuru
Nao Yasuda
Yoshie Murakami
Junya Ushioda
Akiko Kashiwagi
Shingo Suzuki
Kotaro Mori
Bei‐Wen Ying
Tetsuya Yomo
Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli
Molecular Systems Biology
adaptation
gene regulation
monostability
stochastic switching
transciptome
title Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli
title_full Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli
title_fullStr Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli
title_full_unstemmed Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli
title_short Adaptation by stochastic switching of a monostable genetic circuit in Escherichia coli
title_sort adaptation by stochastic switching of a monostable genetic circuit in escherichia coli
topic adaptation
gene regulation
monostability
stochastic switching
transciptome
url https://doi.org/10.1038/msb.2011.24
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