Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage

Abstract Background High-temperature bioethanol production benefits from yeast thermotolerance. Salt stress could induce obvious cross-protection against heat stress of Pichia kudriavzevii, contributing to the improvement of its thermotolerance and bioethanol fermentation. However, the underlying me...

Full description

Bibliographic Details
Main Authors: Chunsheng Li, Qiuying Liu, Yueqi Wang, Xianqing Yang, Shengjun Chen, Yongqiang Zhao, Yanyan Wu, Laihao Li
Format: Article
Language:English
Published: BMC 2021-11-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:https://doi.org/10.1186/s13068-021-02071-0
_version_ 1818534708902887424
author Chunsheng Li
Qiuying Liu
Yueqi Wang
Xianqing Yang
Shengjun Chen
Yongqiang Zhao
Yanyan Wu
Laihao Li
author_facet Chunsheng Li
Qiuying Liu
Yueqi Wang
Xianqing Yang
Shengjun Chen
Yongqiang Zhao
Yanyan Wu
Laihao Li
author_sort Chunsheng Li
collection DOAJ
description Abstract Background High-temperature bioethanol production benefits from yeast thermotolerance. Salt stress could induce obvious cross-protection against heat stress of Pichia kudriavzevii, contributing to the improvement of its thermotolerance and bioethanol fermentation. However, the underlying mechanisms of the cross-protection remain poorly understood. Results Salt stress showed obvious cross-protection for thermotolerance and high-temperature ethanol production of P. kudriavzevii observed by biomass, cell morphology and bioethanol production capacity. The biomass and ethanol production of P. kudriavzevii at 45 °C were, respectively, improved by 2.6 and 3.9 times by 300 mmol/L NaCl. Metabolic network map showed that salt stress obviously improved the key enzymes and intermediates in carbohydrate metabolism, contributing to the synthesis of bioethanol, ATP, amino acids, nucleotides, and unsaturated fatty acids, as well as subsequent intracellular metabolisms. The increasing trehalose, glycerol, HSPs, and ergosterol helped maintain the normal function of cell components. Heat stress induced serious oxidative stress that the ROS-positive cell rate and dead cell rate, respectively, rose from 0.5% and 2.4% to 28.2% and 69.2%, with the incubation temperature increasing from 30 to 45 °C. The heat-induced ROS outburst, oxidative damage, and cell death were obviously inhibited by salt stress, especially the dead cell rate which fell to only 20.3% at 300 mmol/L NaCl. The inhibiting oxidative damage mainly resulted from the abundant synthesis of GSH and GST, which, respectively, increased by 4.8 and 76.1 times after addition of 300 mmol/L NaCl. The improved bioethanol production was not only due to the improved thermotolerance, but resulted from the up-regulated alcohol dehydrogenases and down-regulated aldehyde dehydrogenases by salt stress. Conclusion The results provide a first insight into the mechanisms of the improved thermotolerance and high-temperature bioethanol production of P. kudriavzevii by salt stress, and provide important information to construct genetic engineering yeasts for high-temperature bioethanol production. Graphical Abstract
first_indexed 2024-12-11T18:15:05Z
format Article
id doaj.art-2969cfc3bb8543e19fe5240269be61d2
institution Directory Open Access Journal
issn 1754-6834
language English
last_indexed 2024-12-11T18:15:05Z
publishDate 2021-11-01
publisher BMC
record_format Article
series Biotechnology for Biofuels
spelling doaj.art-2969cfc3bb8543e19fe5240269be61d22022-12-22T00:55:26ZengBMCBiotechnology for Biofuels1754-68342021-11-0114111710.1186/s13068-021-02071-0Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damageChunsheng Li0Qiuying Liu1Yueqi Wang2Xianqing Yang3Shengjun Chen4Yongqiang Zhao5Yanyan Wu6Laihao Li7Key Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesKey Laboratory of Aquatic Product Processing, Ministry of Agriculture and Rural Affairs, National R&D Center for Aquatic Product Processing, South China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesAbstract Background High-temperature bioethanol production benefits from yeast thermotolerance. Salt stress could induce obvious cross-protection against heat stress of Pichia kudriavzevii, contributing to the improvement of its thermotolerance and bioethanol fermentation. However, the underlying mechanisms of the cross-protection remain poorly understood. Results Salt stress showed obvious cross-protection for thermotolerance and high-temperature ethanol production of P. kudriavzevii observed by biomass, cell morphology and bioethanol production capacity. The biomass and ethanol production of P. kudriavzevii at 45 °C were, respectively, improved by 2.6 and 3.9 times by 300 mmol/L NaCl. Metabolic network map showed that salt stress obviously improved the key enzymes and intermediates in carbohydrate metabolism, contributing to the synthesis of bioethanol, ATP, amino acids, nucleotides, and unsaturated fatty acids, as well as subsequent intracellular metabolisms. The increasing trehalose, glycerol, HSPs, and ergosterol helped maintain the normal function of cell components. Heat stress induced serious oxidative stress that the ROS-positive cell rate and dead cell rate, respectively, rose from 0.5% and 2.4% to 28.2% and 69.2%, with the incubation temperature increasing from 30 to 45 °C. The heat-induced ROS outburst, oxidative damage, and cell death were obviously inhibited by salt stress, especially the dead cell rate which fell to only 20.3% at 300 mmol/L NaCl. The inhibiting oxidative damage mainly resulted from the abundant synthesis of GSH and GST, which, respectively, increased by 4.8 and 76.1 times after addition of 300 mmol/L NaCl. The improved bioethanol production was not only due to the improved thermotolerance, but resulted from the up-regulated alcohol dehydrogenases and down-regulated aldehyde dehydrogenases by salt stress. Conclusion The results provide a first insight into the mechanisms of the improved thermotolerance and high-temperature bioethanol production of P. kudriavzevii by salt stress, and provide important information to construct genetic engineering yeasts for high-temperature bioethanol production. Graphical Abstracthttps://doi.org/10.1186/s13068-021-02071-0Pichia kudriavzeviiThermotoleranceBioethanol productionCross-protectionSalt stressMetabolic network
spellingShingle Chunsheng Li
Qiuying Liu
Yueqi Wang
Xianqing Yang
Shengjun Chen
Yongqiang Zhao
Yanyan Wu
Laihao Li
Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
Biotechnology for Biofuels
Pichia kudriavzevii
Thermotolerance
Bioethanol production
Cross-protection
Salt stress
Metabolic network
title Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
title_full Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
title_fullStr Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
title_full_unstemmed Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
title_short Salt stress improves thermotolerance and high-temperature bioethanol production of multi-stress-tolerant Pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
title_sort salt stress improves thermotolerance and high temperature bioethanol production of multi stress tolerant pichia kudriavzevii by stimulating intracellular metabolism and inhibiting oxidative damage
topic Pichia kudriavzevii
Thermotolerance
Bioethanol production
Cross-protection
Salt stress
Metabolic network
url https://doi.org/10.1186/s13068-021-02071-0
work_keys_str_mv AT chunshengli saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT qiuyingliu saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT yueqiwang saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT xianqingyang saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT shengjunchen saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT yongqiangzhao saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT yanyanwu saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage
AT laihaoli saltstressimprovesthermotoleranceandhightemperaturebioethanolproductionofmultistresstolerantpichiakudriavzeviibystimulatingintracellularmetabolismandinhibitingoxidativedamage