Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization

Microbial butanol production is an important sustainable energy option, but it is economically limited by poor process performance. Butanol is toxic and damages bacterial cell membranes, requiring cells to expend energy for survival rather than for butanol production. Here we explore the utility of...

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Main Authors: Chia, Geraldine Wan Ni, Seviour, Thomas, Kjelleberg, Staffan, Hinks, Jamie
Other Authors: Interdisciplinary Graduate School (IGS)
Format: Article
Language:English
Published: 2022
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Online Access:https://hdl.handle.net/10356/160003
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Institution: Nanyang Technological University
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spelling sg-ntu-dr.10356-1600032022-07-07T06:53:38Z Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization Chia, Geraldine Wan Ni Seviour, Thomas Kjelleberg, Staffan Hinks, Jamie Interdisciplinary Graduate School (IGS) Singapore Centre for Environmental Life Sciences and Engineering Engineering::Environmental engineering Xanthophyll Pigments Lutein Beta-Carotene Microbial butanol production is an important sustainable energy option, but it is economically limited by poor process performance. Butanol is toxic and damages bacterial cell membranes, requiring cells to expend energy for survival rather than for butanol production. Here we explore the utility of two polar carotenoids, lutein (LUT) and zeaxanthin (ZEA), as molecular rivets to mitigate membrane fluidization by solvents and thus improve butanol tolerance in Escherichia coli. LUT and ZEA formed carotenoid-rich nanodomains in multilamellar vesicles, at molar ratios of 1 : 9 relative to phospholipids (10 mol%), which reduced the fluidization effect of 3.5% (v/v) butanol by 62%, as indicated by changes in generalized polarization values of the membrane fluidity probe, Laurdan. Additionally, membrane penetration of butanol was 38% lower in the same test system. In carotenoid-treated E. coli, butanol-induced membrane damage, determined by propidium iodide, decreased by up to 30%. Additionally, E. coli treated with both LUT and ZEA achieved a two-log increase in cell viability upon acute butanol exposure of 3.5% (v/v), compared to untreated cells. This is the first time that carotenoids have been used to fortify cellular membranes and reduce biomass loss due to butanol, thereby revealing a potential biotechnological application for carotenoids to improve the economics of microbial butanol production. Ministry of Education (MOE) Nanyang Technological University National Research Foundation (NRF) Funding for this work was provided through Ministry of Education Singapore AcRF Tier 2 grant number MOE2016-T2-1-148. SCELSE is funded by Singapore's Ministry of Education, National Research Foundation, Nanyang Technological University (NTU), and National University of Singapore (NUS) and hosted by NTU in partnership with NUS. 2022-07-07T06:53:38Z 2022-07-07T06:53:38Z 2021 Journal Article Chia, G. W. N., Seviour, T., Kjelleberg, S. & Hinks, J. (2021). Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization. Environmental Science: Nano, 8(1), 328-341. https://dx.doi.org/10.1039/D0EN00983K 2051-8153 https://hdl.handle.net/10356/160003 10.1039/D0EN00983K 1 8 328 341 en MOE2016-T2-1-148 Environmental Science: Nano © 2021 The Royal Society of Chemistry. All rights reserved.
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Engineering::Environmental engineering
Xanthophyll Pigments Lutein
Beta-Carotene
spellingShingle Engineering::Environmental engineering
Xanthophyll Pigments Lutein
Beta-Carotene
Chia, Geraldine Wan Ni
Seviour, Thomas
Kjelleberg, Staffan
Hinks, Jamie
Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
description Microbial butanol production is an important sustainable energy option, but it is economically limited by poor process performance. Butanol is toxic and damages bacterial cell membranes, requiring cells to expend energy for survival rather than for butanol production. Here we explore the utility of two polar carotenoids, lutein (LUT) and zeaxanthin (ZEA), as molecular rivets to mitigate membrane fluidization by solvents and thus improve butanol tolerance in Escherichia coli. LUT and ZEA formed carotenoid-rich nanodomains in multilamellar vesicles, at molar ratios of 1 : 9 relative to phospholipids (10 mol%), which reduced the fluidization effect of 3.5% (v/v) butanol by 62%, as indicated by changes in generalized polarization values of the membrane fluidity probe, Laurdan. Additionally, membrane penetration of butanol was 38% lower in the same test system. In carotenoid-treated E. coli, butanol-induced membrane damage, determined by propidium iodide, decreased by up to 30%. Additionally, E. coli treated with both LUT and ZEA achieved a two-log increase in cell viability upon acute butanol exposure of 3.5% (v/v), compared to untreated cells. This is the first time that carotenoids have been used to fortify cellular membranes and reduce biomass loss due to butanol, thereby revealing a potential biotechnological application for carotenoids to improve the economics of microbial butanol production.
author2 Interdisciplinary Graduate School (IGS)
author_facet Interdisciplinary Graduate School (IGS)
Chia, Geraldine Wan Ni
Seviour, Thomas
Kjelleberg, Staffan
Hinks, Jamie
format Article
author Chia, Geraldine Wan Ni
Seviour, Thomas
Kjelleberg, Staffan
Hinks, Jamie
author_sort Chia, Geraldine Wan Ni
title Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
title_short Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
title_full Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
title_fullStr Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
title_full_unstemmed Carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
title_sort carotenoids improve bacterial tolerance towards biobutanol through membrane stabilization
publishDate 2022
url https://hdl.handle.net/10356/160003
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