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Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae

BACKGROUND: Saccharomyces cerevisiae wild strains generally have poor xylose-utilization capability, which is a major barrier for efficient bioconversion of lignocellulosic biomass. Laboratory adaption is commonly used to enhance xylose utilization of recombinant S. cerevisiae. Apparently, yeast cel...

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Autores principales: Cheng, Cheng, Tang, Rui-Qi, Xiong, Liang, Hector, Ronald E., Bai, Feng-Wu, Zhao, Xin-Qing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5798184/
https://www.ncbi.nlm.nih.gov/pubmed/29441126
http://dx.doi.org/10.1186/s13068-018-1018-y
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author Cheng, Cheng
Tang, Rui-Qi
Xiong, Liang
Hector, Ronald E.
Bai, Feng-Wu
Zhao, Xin-Qing
author_facet Cheng, Cheng
Tang, Rui-Qi
Xiong, Liang
Hector, Ronald E.
Bai, Feng-Wu
Zhao, Xin-Qing
author_sort Cheng, Cheng
collection PubMed
description BACKGROUND: Saccharomyces cerevisiae wild strains generally have poor xylose-utilization capability, which is a major barrier for efficient bioconversion of lignocellulosic biomass. Laboratory adaption is commonly used to enhance xylose utilization of recombinant S. cerevisiae. Apparently, yeast cells could remodel the metabolic network for xylose metabolism. However, it still remains unclear why natural isolates of S. cerevisiae poorly utilize xylose. Here, we analyzed a unique S. cerevisiae natural isolate YB-2625 which has superior xylose metabolism capability in the presence of mixed-sugar. Comparative transcriptomic analysis was performed using S. cerevisiae YB-2625 grown in a mixture of glucose and xylose, and the model yeast strain S288C served as a control. Global gene transcription was compared at both the early mixed-sugar utilization stage and the latter xylose-utilization stage. RESULTS: Genes involved in endogenous xylose-assimilation (XYL2 and XKS1), gluconeogenesis, and TCA cycle showed higher transcription levels in S. cerevisiae YB-2625 at the xylose-utilization stage, when compared to the reference strain. On the other hand, transcription factor encoding genes involved in regulation of glucose repression (MIG1, MIG2, and MIG3) as well as HXK2 displayed decreased transcriptional levels in YB-2625, suggesting the alleviation of glucose repression of S. cerevisiae YB-2625. Notably, genes encoding antioxidant enzymes (CTT1, CTA1, SOD2, and PRX1) showed higher transcription levels in S. cerevisiae YB-2625 in the xylose-utilization stage than that of the reference strain. Consistently, catalase activity of YB-2625 was 1.9-fold higher than that of S. cerevisiae S288C during the xylose-utilization stage. As a result, intracellular reactive oxygen species levels of S. cerevisiae YB-2625 were 43.3 and 58.6% lower than that of S288C at both sugar utilization stages. Overexpression of CTT1 and PRX1 in the recombinant strain S. cerevisiae YRH396 deriving from S. cerevisiae YB-2625 increased cell growth when xylose was used as the sole carbon source, leading to 13.5 and 18.1%, respectively, more xylose consumption. CONCLUSIONS: Enhanced oxidative stress tolerance and relief of glucose repression are proposed to be two major mechanisms for superior xylose utilization by S. cerevisiae YB-2625. The present study provides insights into the innate regulatory mechanisms underlying xylose utilization in wild-type S. cerevisiae, which benefits the rapid development of robust yeast strains for lignocellulosic biorefineries. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1018-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-57981842018-02-13 Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae Cheng, Cheng Tang, Rui-Qi Xiong, Liang Hector, Ronald E. Bai, Feng-Wu Zhao, Xin-Qing Biotechnol Biofuels Research BACKGROUND: Saccharomyces cerevisiae wild strains generally have poor xylose-utilization capability, which is a major barrier for efficient bioconversion of lignocellulosic biomass. Laboratory adaption is commonly used to enhance xylose utilization of recombinant S. cerevisiae. Apparently, yeast cells could remodel the metabolic network for xylose metabolism. However, it still remains unclear why natural isolates of S. cerevisiae poorly utilize xylose. Here, we analyzed a unique S. cerevisiae natural isolate YB-2625 which has superior xylose metabolism capability in the presence of mixed-sugar. Comparative transcriptomic analysis was performed using S. cerevisiae YB-2625 grown in a mixture of glucose and xylose, and the model yeast strain S288C served as a control. Global gene transcription was compared at both the early mixed-sugar utilization stage and the latter xylose-utilization stage. RESULTS: Genes involved in endogenous xylose-assimilation (XYL2 and XKS1), gluconeogenesis, and TCA cycle showed higher transcription levels in S. cerevisiae YB-2625 at the xylose-utilization stage, when compared to the reference strain. On the other hand, transcription factor encoding genes involved in regulation of glucose repression (MIG1, MIG2, and MIG3) as well as HXK2 displayed decreased transcriptional levels in YB-2625, suggesting the alleviation of glucose repression of S. cerevisiae YB-2625. Notably, genes encoding antioxidant enzymes (CTT1, CTA1, SOD2, and PRX1) showed higher transcription levels in S. cerevisiae YB-2625 in the xylose-utilization stage than that of the reference strain. Consistently, catalase activity of YB-2625 was 1.9-fold higher than that of S. cerevisiae S288C during the xylose-utilization stage. As a result, intracellular reactive oxygen species levels of S. cerevisiae YB-2625 were 43.3 and 58.6% lower than that of S288C at both sugar utilization stages. Overexpression of CTT1 and PRX1 in the recombinant strain S. cerevisiae YRH396 deriving from S. cerevisiae YB-2625 increased cell growth when xylose was used as the sole carbon source, leading to 13.5 and 18.1%, respectively, more xylose consumption. CONCLUSIONS: Enhanced oxidative stress tolerance and relief of glucose repression are proposed to be two major mechanisms for superior xylose utilization by S. cerevisiae YB-2625. The present study provides insights into the innate regulatory mechanisms underlying xylose utilization in wild-type S. cerevisiae, which benefits the rapid development of robust yeast strains for lignocellulosic biorefineries. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1018-y) contains supplementary material, which is available to authorized users. BioMed Central 2018-02-05 /pmc/articles/PMC5798184/ /pubmed/29441126 http://dx.doi.org/10.1186/s13068-018-1018-y Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Cheng, Cheng
Tang, Rui-Qi
Xiong, Liang
Hector, Ronald E.
Bai, Feng-Wu
Zhao, Xin-Qing
Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae
title Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae
title_full Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae
title_fullStr Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae
title_full_unstemmed Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae
title_short Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae
title_sort association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of saccharomyces cerevisiae
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5798184/
https://www.ncbi.nlm.nih.gov/pubmed/29441126
http://dx.doi.org/10.1186/s13068-018-1018-y
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