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Escherichia coli displays a conserved membrane proteomic response to a range of alcohols

BACKGROUND: Alcohol is a good and environment-friendly fuel that can be microbially produced, capable of eliminating many of the limitations of the present-day fossil fuels. However, the inherent toxic nature of alcohols to the microbial cells leads to end-product inhibition that limits large-scale...

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Autores principales: Sen, Oishi, Hinks, Jamie, Lin, Qifeng, Lin, Qingsong, Kjelleberg, Staffan, Rice, Scott A., Seviour, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10546733/
https://www.ncbi.nlm.nih.gov/pubmed/37789404
http://dx.doi.org/10.1186/s13068-023-02401-4
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author Sen, Oishi
Hinks, Jamie
Lin, Qifeng
Lin, Qingsong
Kjelleberg, Staffan
Rice, Scott A.
Seviour, Thomas
author_facet Sen, Oishi
Hinks, Jamie
Lin, Qifeng
Lin, Qingsong
Kjelleberg, Staffan
Rice, Scott A.
Seviour, Thomas
author_sort Sen, Oishi
collection PubMed
description BACKGROUND: Alcohol is a good and environment-friendly fuel that can be microbially produced, capable of eliminating many of the limitations of the present-day fossil fuels. However, the inherent toxic nature of alcohols to the microbial cells leads to end-product inhibition that limits large-scale alcohol production by fermentation. Fundamental knowledge about the stress responses of microorganisms to alcohols would greatly facilitate to improve the microbial alcohol tolerance. The current study elucidates and compares the changes in the membrane proteome of Escherichia coli in response to a range of alcohols. RESULTS: Although alcohol toxicity increased exponentially with alcohol chain length (2–6 carbon), similar stress responses were observed in the inner and outer membrane proteome of E. coli in the presence of 2-, 4- and 6-carbon alcohols at the MIC(50). This pertains to: (1) increased levels of inner membrane transporters for uptake of energy-producing metabolites, (2) reduced levels of non-essential proteins, associated with anaerobic, carbon starvation and osmotic stress, for energy conservation, (3) increased levels of murein degrading enzymes (MltA, EmtA, MliC and DigH) promoting cell elongation and 4) reduced levels of most outer membrane β-barrel proteins (LptD, FadL, LamB, TolC and BamA). Major outer membrane β-barrel protein OmpC, which is known to contribute to ethanol tolerance and membrane integrity, was notably reduced by alcohol stress. While LPS is important for OmpC trimerisation, LPS release by EDTA did not lower OmpC levels. This suggests that LPS release, which is reported under alcohol stress, does not contribute to the reduced levels of OmpC in the presence of alcohol. CONCLUSIONS: Since alcohol primarily targets the integrity of the membrane, maintenance of outer membrane OmpC levels in the presence of alcohol might help in the survival of E. coli to higher alcohol concentrations. The study provides important information about the membrane protein responses of E. coli to a range of alcohols, which can be used to develop targeted strategies for increased microbial alcohol tolerance and hence bioalcohol production. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02401-4.
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spelling pubmed-105467332023-10-04 Escherichia coli displays a conserved membrane proteomic response to a range of alcohols Sen, Oishi Hinks, Jamie Lin, Qifeng Lin, Qingsong Kjelleberg, Staffan Rice, Scott A. Seviour, Thomas Biotechnol Biofuels Bioprod Research BACKGROUND: Alcohol is a good and environment-friendly fuel that can be microbially produced, capable of eliminating many of the limitations of the present-day fossil fuels. However, the inherent toxic nature of alcohols to the microbial cells leads to end-product inhibition that limits large-scale alcohol production by fermentation. Fundamental knowledge about the stress responses of microorganisms to alcohols would greatly facilitate to improve the microbial alcohol tolerance. The current study elucidates and compares the changes in the membrane proteome of Escherichia coli in response to a range of alcohols. RESULTS: Although alcohol toxicity increased exponentially with alcohol chain length (2–6 carbon), similar stress responses were observed in the inner and outer membrane proteome of E. coli in the presence of 2-, 4- and 6-carbon alcohols at the MIC(50). This pertains to: (1) increased levels of inner membrane transporters for uptake of energy-producing metabolites, (2) reduced levels of non-essential proteins, associated with anaerobic, carbon starvation and osmotic stress, for energy conservation, (3) increased levels of murein degrading enzymes (MltA, EmtA, MliC and DigH) promoting cell elongation and 4) reduced levels of most outer membrane β-barrel proteins (LptD, FadL, LamB, TolC and BamA). Major outer membrane β-barrel protein OmpC, which is known to contribute to ethanol tolerance and membrane integrity, was notably reduced by alcohol stress. While LPS is important for OmpC trimerisation, LPS release by EDTA did not lower OmpC levels. This suggests that LPS release, which is reported under alcohol stress, does not contribute to the reduced levels of OmpC in the presence of alcohol. CONCLUSIONS: Since alcohol primarily targets the integrity of the membrane, maintenance of outer membrane OmpC levels in the presence of alcohol might help in the survival of E. coli to higher alcohol concentrations. The study provides important information about the membrane protein responses of E. coli to a range of alcohols, which can be used to develop targeted strategies for increased microbial alcohol tolerance and hence bioalcohol production. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13068-023-02401-4. BioMed Central 2023-10-03 /pmc/articles/PMC10546733/ /pubmed/37789404 http://dx.doi.org/10.1186/s13068-023-02401-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Sen, Oishi
Hinks, Jamie
Lin, Qifeng
Lin, Qingsong
Kjelleberg, Staffan
Rice, Scott A.
Seviour, Thomas
Escherichia coli displays a conserved membrane proteomic response to a range of alcohols
title Escherichia coli displays a conserved membrane proteomic response to a range of alcohols
title_full Escherichia coli displays a conserved membrane proteomic response to a range of alcohols
title_fullStr Escherichia coli displays a conserved membrane proteomic response to a range of alcohols
title_full_unstemmed Escherichia coli displays a conserved membrane proteomic response to a range of alcohols
title_short Escherichia coli displays a conserved membrane proteomic response to a range of alcohols
title_sort escherichia coli displays a conserved membrane proteomic response to a range of alcohols
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10546733/
https://www.ncbi.nlm.nih.gov/pubmed/37789404
http://dx.doi.org/10.1186/s13068-023-02401-4
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