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Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter
INTRODUCTION: The molecular links between shock-response and adaptation remain poorly understood, particularly for extremophiles. This has hindered rational engineering of solvent tolerance and correlated traits (e.g., productivity) in extremophiles. To untangle such molecular links, here we establi...
Autores principales: | , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2013
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3751872/ https://www.ncbi.nlm.nih.gov/pubmed/23875846 http://dx.doi.org/10.1186/1754-6834-6-103 |
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author | Lin, Lu Ji, Yuetong Tu, Qichao Huang, Ranran Teng, Lin Zeng, Xiaowei Song, Houhui Wang, Kun Zhou, Qian Li, Yifei Cui, Qiu He, Zhili Zhou, Jizhong Xu, Jian |
author_facet | Lin, Lu Ji, Yuetong Tu, Qichao Huang, Ranran Teng, Lin Zeng, Xiaowei Song, Houhui Wang, Kun Zhou, Qian Li, Yifei Cui, Qiu He, Zhili Zhou, Jizhong Xu, Jian |
author_sort | Lin, Lu |
collection | PubMed |
description | INTRODUCTION: The molecular links between shock-response and adaptation remain poorly understood, particularly for extremophiles. This has hindered rational engineering of solvent tolerance and correlated traits (e.g., productivity) in extremophiles. To untangle such molecular links, here we established a model that tracked the microevolution from shock to adaptation in thermophilic bacteria. METHOD: Temporal dynamics of genomes and transcriptomes was tracked for Thermoanaerobacter sp. X514 which under increasing exogenous ethanol evolved from ethanol-sensitive wild-type (Strain X) to tolerance of 2%- (X(I)) and eventually 6%-ethanol (X(II)). Based on the reconstructed transcriptional network underlying stress tolerance, genetic engineering was employed to improve ethanol tolerance and production in Thermoanaerobacter. RESULTS: The spontaneous genome mutation rate (μ(g)) of Thermoanaerobacter sp. X514, calculated at 0.045, suggested a higher mutation rate in thermophile than previously thought. Transcriptomic comparison revealed that shock-response and adaptation were distinct in nature, whereas the transcriptomes of X(II) resembled those of the extendedly shocked X. To respond to ethanol shock, X employed fructose-specific phosphotransferase system (PTS), Arginine Deiminase (ADI) pathway, alcohol dehydrogenase (Adh) and a distinct mechanism of V-type ATPase. As an adaptation to exogenous ethanol, X(I) mobilized resistance-nodulation-cell division (RND) efflux system and Adh, whereas X(II,) which produced higher ethanol than X(I), employed ECF-type ϭ(24), an alcohol catabolism operon and phase-specific heat-shock proteins (Hsps), modulated hexose/pentose-transport operon structure and reinforced membrane rigidity. Exploiting these findings, we further showed that ethanol productivity and tolerance can be improved simultaneously by overexpressing adh or ϭ(24) in X. CONCLUSION: Our work revealed thermophilic-bacteria specific features of adaptive evolution and demonstrated a rational strategy to engineer co-evolving industrial traits. As improvements of shock-response, stress tolerance and productivity have been crucial aims in industrial applications employing thermophiles, our findings should be valuable not just to the production of ethanol but also to a wide variety of biofuels and biochemicals. |
format | Online Article Text |
id | pubmed-3751872 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2013 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-37518722013-08-24 Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter Lin, Lu Ji, Yuetong Tu, Qichao Huang, Ranran Teng, Lin Zeng, Xiaowei Song, Houhui Wang, Kun Zhou, Qian Li, Yifei Cui, Qiu He, Zhili Zhou, Jizhong Xu, Jian Biotechnol Biofuels Research INTRODUCTION: The molecular links between shock-response and adaptation remain poorly understood, particularly for extremophiles. This has hindered rational engineering of solvent tolerance and correlated traits (e.g., productivity) in extremophiles. To untangle such molecular links, here we established a model that tracked the microevolution from shock to adaptation in thermophilic bacteria. METHOD: Temporal dynamics of genomes and transcriptomes was tracked for Thermoanaerobacter sp. X514 which under increasing exogenous ethanol evolved from ethanol-sensitive wild-type (Strain X) to tolerance of 2%- (X(I)) and eventually 6%-ethanol (X(II)). Based on the reconstructed transcriptional network underlying stress tolerance, genetic engineering was employed to improve ethanol tolerance and production in Thermoanaerobacter. RESULTS: The spontaneous genome mutation rate (μ(g)) of Thermoanaerobacter sp. X514, calculated at 0.045, suggested a higher mutation rate in thermophile than previously thought. Transcriptomic comparison revealed that shock-response and adaptation were distinct in nature, whereas the transcriptomes of X(II) resembled those of the extendedly shocked X. To respond to ethanol shock, X employed fructose-specific phosphotransferase system (PTS), Arginine Deiminase (ADI) pathway, alcohol dehydrogenase (Adh) and a distinct mechanism of V-type ATPase. As an adaptation to exogenous ethanol, X(I) mobilized resistance-nodulation-cell division (RND) efflux system and Adh, whereas X(II,) which produced higher ethanol than X(I), employed ECF-type ϭ(24), an alcohol catabolism operon and phase-specific heat-shock proteins (Hsps), modulated hexose/pentose-transport operon structure and reinforced membrane rigidity. Exploiting these findings, we further showed that ethanol productivity and tolerance can be improved simultaneously by overexpressing adh or ϭ(24) in X. CONCLUSION: Our work revealed thermophilic-bacteria specific features of adaptive evolution and demonstrated a rational strategy to engineer co-evolving industrial traits. As improvements of shock-response, stress tolerance and productivity have been crucial aims in industrial applications employing thermophiles, our findings should be valuable not just to the production of ethanol but also to a wide variety of biofuels and biochemicals. BioMed Central 2013-07-22 /pmc/articles/PMC3751872/ /pubmed/23875846 http://dx.doi.org/10.1186/1754-6834-6-103 Text en Copyright © 2013 Lin et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Research Lin, Lu Ji, Yuetong Tu, Qichao Huang, Ranran Teng, Lin Zeng, Xiaowei Song, Houhui Wang, Kun Zhou, Qian Li, Yifei Cui, Qiu He, Zhili Zhou, Jizhong Xu, Jian Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter |
title | Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter |
title_full | Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter |
title_fullStr | Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter |
title_full_unstemmed | Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter |
title_short | Microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in Thermoanaerobacter |
title_sort | microevolution from shock to adaptation revealed strategies improving ethanol tolerance and production in thermoanaerobacter |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3751872/ https://www.ncbi.nlm.nih.gov/pubmed/23875846 http://dx.doi.org/10.1186/1754-6834-6-103 |
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