Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering

Oxidative stress is a major stress type observed in yeast bioprocesses, resulting in a decrease in yeast growth, viability, and productivity. Thus, robust yeast strains with increased resistance to oxidative stress are in highly demand by the industry. In addition, oxidative stress is also associate...

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Main Authors: Nazlı Kocaefe-Özşen, Bahtiyar Yilmaz, Ceren Alkım, Mevlüt Arslan, Alican Topaloğlu, Halil l̇brahim Kısakesen, Erdinç Gülsev, Z. Petek Çakar
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.822864/full
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author Nazlı Kocaefe-Özşen
Nazlı Kocaefe-Özşen
Bahtiyar Yilmaz
Bahtiyar Yilmaz
Ceren Alkım
Ceren Alkım
Mevlüt Arslan
Mevlüt Arslan
Alican Topaloğlu
Alican Topaloğlu
Halil l̇brahim Kısakesen
Halil l̇brahim Kısakesen
Erdinç Gülsev
Erdinç Gülsev
Z. Petek Çakar
Z. Petek Çakar
author_facet Nazlı Kocaefe-Özşen
Nazlı Kocaefe-Özşen
Bahtiyar Yilmaz
Bahtiyar Yilmaz
Ceren Alkım
Ceren Alkım
Mevlüt Arslan
Mevlüt Arslan
Alican Topaloğlu
Alican Topaloğlu
Halil l̇brahim Kısakesen
Halil l̇brahim Kısakesen
Erdinç Gülsev
Erdinç Gülsev
Z. Petek Çakar
Z. Petek Çakar
author_sort Nazlı Kocaefe-Özşen
collection DOAJ
description Oxidative stress is a major stress type observed in yeast bioprocesses, resulting in a decrease in yeast growth, viability, and productivity. Thus, robust yeast strains with increased resistance to oxidative stress are in highly demand by the industry. In addition, oxidative stress is also associated with aging and age-related complex conditions such as cancer and neurodegenerative diseases. Saccharomyces cerevisiae, as a model eukaryote, has been used to study these complex eukaryotic processes. However, the molecular mechanisms underlying oxidative stress responses and resistance are unclear. In this study, we have employed evolutionary engineering (also known as adaptive laboratory evolution – ALE) strategies to obtain an oxidative stress-resistant and genetically stable S. cerevisiae strain. Comparative physiological, transcriptomic, and genomic analyses of the evolved strain were then performed with respect to the reference strain. The results show that the oxidative stress-resistant evolved strain was also cross-resistant against other types of stressors, including heat, freeze-thaw, ethanol, cobalt, iron, and salt. It was also found to have higher levels of trehalose and glycogen production. Further, comparative transcriptomic analysis showed an upregulation of many genes associated with the stress response, transport, carbohydrate, lipid and cofactor metabolic processes, protein phosphorylation, cell wall organization, and biogenesis. Genes that were downregulated included those related to ribosome and RNA processing, nuclear transport, tRNA, and cell cycle. Whole genome re-sequencing analysis of the evolved strain identified mutations in genes related to the stress response, cell wall organization, carbohydrate metabolism/transport, which are in line with the physiological and transcriptomic results, and may give insight toward the complex molecular mechanisms of oxidative stress resistance.
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spelling doaj.art-c51f53ce7bb44bf7a6081648aca25cd42022-12-21T20:21:01ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-02-011310.3389/fmicb.2022.822864822864Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary EngineeringNazlı Kocaefe-Özşen0Nazlı Kocaefe-Özşen1Bahtiyar Yilmaz2Bahtiyar Yilmaz3Ceren Alkım4Ceren Alkım5Mevlüt Arslan6Mevlüt Arslan7Alican Topaloğlu8Alican Topaloğlu9Halil l̇brahim Kısakesen10Halil l̇brahim Kısakesen11Erdinç Gülsev12Erdinç Gülsev13Z. Petek Çakar14Z. Petek Çakar15Department of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyDepartment of Molecular Biology and Genetics, Istanbul Technical University, Istanbul, TurkeyDr. Orhan Öcalgiray Molecular Biology, Biotechnology and Genetics Research Center (ITU-MOBGAM), Istanbul Technical University, Istanbul, TurkeyOxidative stress is a major stress type observed in yeast bioprocesses, resulting in a decrease in yeast growth, viability, and productivity. Thus, robust yeast strains with increased resistance to oxidative stress are in highly demand by the industry. In addition, oxidative stress is also associated with aging and age-related complex conditions such as cancer and neurodegenerative diseases. Saccharomyces cerevisiae, as a model eukaryote, has been used to study these complex eukaryotic processes. However, the molecular mechanisms underlying oxidative stress responses and resistance are unclear. In this study, we have employed evolutionary engineering (also known as adaptive laboratory evolution – ALE) strategies to obtain an oxidative stress-resistant and genetically stable S. cerevisiae strain. Comparative physiological, transcriptomic, and genomic analyses of the evolved strain were then performed with respect to the reference strain. The results show that the oxidative stress-resistant evolved strain was also cross-resistant against other types of stressors, including heat, freeze-thaw, ethanol, cobalt, iron, and salt. It was also found to have higher levels of trehalose and glycogen production. Further, comparative transcriptomic analysis showed an upregulation of many genes associated with the stress response, transport, carbohydrate, lipid and cofactor metabolic processes, protein phosphorylation, cell wall organization, and biogenesis. Genes that were downregulated included those related to ribosome and RNA processing, nuclear transport, tRNA, and cell cycle. Whole genome re-sequencing analysis of the evolved strain identified mutations in genes related to the stress response, cell wall organization, carbohydrate metabolism/transport, which are in line with the physiological and transcriptomic results, and may give insight toward the complex molecular mechanisms of oxidative stress resistance.https://www.frontiersin.org/articles/10.3389/fmicb.2022.822864/fulloxidative stressreactive oxygen speciesevolutionary engineeringstress resistanceheat preconditioningSaccharomyces cerevisiae
spellingShingle Nazlı Kocaefe-Özşen
Nazlı Kocaefe-Özşen
Bahtiyar Yilmaz
Bahtiyar Yilmaz
Ceren Alkım
Ceren Alkım
Mevlüt Arslan
Mevlüt Arslan
Alican Topaloğlu
Alican Topaloğlu
Halil l̇brahim Kısakesen
Halil l̇brahim Kısakesen
Erdinç Gülsev
Erdinç Gülsev
Z. Petek Çakar
Z. Petek Çakar
Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering
Frontiers in Microbiology
oxidative stress
reactive oxygen species
evolutionary engineering
stress resistance
heat preconditioning
Saccharomyces cerevisiae
title Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering
title_full Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering
title_fullStr Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering
title_full_unstemmed Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering
title_short Physiological and Molecular Characterization of an Oxidative Stress-Resistant Saccharomyces cerevisiae Strain Obtained by Evolutionary Engineering
title_sort physiological and molecular characterization of an oxidative stress resistant saccharomyces cerevisiae strain obtained by evolutionary engineering
topic oxidative stress
reactive oxygen species
evolutionary engineering
stress resistance
heat preconditioning
Saccharomyces cerevisiae
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.822864/full
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