Response mechanisms of different Saccharomyces cerevisiae strains to succinic acid.
Saccharomyces cerevisiae
Comparative transcriptomic analysis
Genetic background
Response mechanism
Succinic acid
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
08 May 2024
08 May 2024
Historique:
received:
27
10
2023
accepted:
25
04
2024
medline:
9
5
2024
pubmed:
9
5
2024
entrez:
9
5
2024
Statut:
epublish
Résumé
The production of succinic acid (SA) from biomass has attracted worldwide interest. Saccharomyces cerevisiae is preferred for SA production due to its strong tolerance to low pH conditions, ease of genetic manipulation, and extensive application in industrial processes. However, when compared with bacterial producers, the SA titers and productivities achieved by engineered S. cerevisiae strains were relatively low. To develop efficient SA-producing strains, it's necessary to clearly understand how S. cerevisiae cells respond to SA. In this study, we cultivated five S. cerevisiae strains with different genetic backgrounds under different concentrations of SA. Among them, KF7 and NBRC1958 demonstrated high tolerance to SA, whereas NBRC2018 displayed the least tolerance. Therefore, these three strains were chosen to study how S. cerevisiae responds to SA. Under a concentration of 20 g/L SA, only a few differentially expressed genes were observed in three strains. At the higher concentration of 60 g/L SA, the response mechanisms of the three strains diverged notably. For KF7, genes involved in the glyoxylate cycle were significantly downregulated, whereas genes involved in gluconeogenesis, the pentose phosphate pathway, protein folding, and meiosis were significantly upregulated. For NBRC1958, genes related to the biosynthesis of vitamin B6, thiamin, and purine were significantly downregulated, whereas genes related to protein folding, toxin efflux, and cell wall remodeling were significantly upregulated. For NBRC2018, there was a significant upregulation of genes connected to the pentose phosphate pathway, gluconeogenesis, fatty acid utilization, and protein folding, except for the small heat shock protein gene HSP26. Overexpression of HSP26 and HSP42 notably enhanced the cell growth of NBRC1958 both in the presence and absence of SA. The inherent activities of small heat shock proteins, the levels of acetyl-CoA and the strains' potential capacity to consume SA all seem to affect the responses and tolerances of S. cerevisiae strains to SA. These factors should be taken into consideration when choosing host strains for SA production. This study provides a theoretical basis and identifies potential host strains for the development of robust and efficient SA-producing strains.
Sections du résumé
BACKGROUND
BACKGROUND
The production of succinic acid (SA) from biomass has attracted worldwide interest. Saccharomyces cerevisiae is preferred for SA production due to its strong tolerance to low pH conditions, ease of genetic manipulation, and extensive application in industrial processes. However, when compared with bacterial producers, the SA titers and productivities achieved by engineered S. cerevisiae strains were relatively low. To develop efficient SA-producing strains, it's necessary to clearly understand how S. cerevisiae cells respond to SA.
RESULTS
RESULTS
In this study, we cultivated five S. cerevisiae strains with different genetic backgrounds under different concentrations of SA. Among them, KF7 and NBRC1958 demonstrated high tolerance to SA, whereas NBRC2018 displayed the least tolerance. Therefore, these three strains were chosen to study how S. cerevisiae responds to SA. Under a concentration of 20 g/L SA, only a few differentially expressed genes were observed in three strains. At the higher concentration of 60 g/L SA, the response mechanisms of the three strains diverged notably. For KF7, genes involved in the glyoxylate cycle were significantly downregulated, whereas genes involved in gluconeogenesis, the pentose phosphate pathway, protein folding, and meiosis were significantly upregulated. For NBRC1958, genes related to the biosynthesis of vitamin B6, thiamin, and purine were significantly downregulated, whereas genes related to protein folding, toxin efflux, and cell wall remodeling were significantly upregulated. For NBRC2018, there was a significant upregulation of genes connected to the pentose phosphate pathway, gluconeogenesis, fatty acid utilization, and protein folding, except for the small heat shock protein gene HSP26. Overexpression of HSP26 and HSP42 notably enhanced the cell growth of NBRC1958 both in the presence and absence of SA.
CONCLUSIONS
CONCLUSIONS
The inherent activities of small heat shock proteins, the levels of acetyl-CoA and the strains' potential capacity to consume SA all seem to affect the responses and tolerances of S. cerevisiae strains to SA. These factors should be taken into consideration when choosing host strains for SA production. This study provides a theoretical basis and identifies potential host strains for the development of robust and efficient SA-producing strains.
Identifiants
pubmed: 38720268
doi: 10.1186/s12866-024-03314-4
pii: 10.1186/s12866-024-03314-4
doi:
Substances chimiques
Succinic Acid
AB6MNQ6J6L
Saccharomyces cerevisiae Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
158Subventions
Organisme : National Natural Science Foundation of China
ID : 52300169
Organisme : National Key Research and Development Program of China
ID : 2022YFE0108500
Informations de copyright
© 2024. The Author(s).
Références
Ahn JH, Jang YS, Lee SY. Production of succinic acid by metabolically engineered microorganisms. Curr Opin Biotechnol. 2016;42:54–66.
pubmed: 26990278
doi: 10.1016/j.copbio.2016.02.034
McKinlay JB, Vieille C, Zeikus JG. Prospects for a bio-based succinate industry. Appl Microbiol Biotechnol. 2007;76(4):727–40.
pubmed: 17609945
doi: 10.1007/s00253-007-1057-y
Li Q, Yang M, Wang D, Li W, Wu Y, Zhang Y, Xing J, Su Z. Efficient conversion of crop stalk wastes into succinic acid production by Actinobacillus succinogenes. Bioresour Technol. 2010;101(9):3292–4.
pubmed: 20061143
doi: 10.1016/j.biortech.2009.12.064
Lee SY, Kim JM, Song H, Lee JW, Kim TY, Jang YS. From genome sequence to integrated bioprocess for succinic acid production by Mannheimia succiniciproducens. Appl Microbiol Biotechnol. 2008;79(1):11–22.
pubmed: 18340442
doi: 10.1007/s00253-008-1424-3
Okino S, Noburyu R, Suda M, Jojima T, Inui M, Yukawa H. An efficient succinic acid production process in a metabolically engineered Corynebacterium glutamicum strain. Appl Microbiol Biotechnol. 2008;81(3):459–64.
pubmed: 18777022
doi: 10.1007/s00253-008-1668-y
Cimini D, Argenzio O, D’Ambrosio S, Lama L, Finore I, Finamore R, Pepe O, Faraco V, Schiraldi C. Production of succinic acid from Basfia succiniciproducens up to the pilot scale from Arundo donax hydrolysate. Bioresour Technol. 2016;222:355–60.
pubmed: 27741473
doi: 10.1016/j.biortech.2016.10.004
Podlesny M, Jarocki P, Wyrostek J, Czernecki T, Kucharska J, Nowak A, Targonski Z. Enterobacter Sp LU1 as a novel succinic acid producer - co-utilization of glycerol and lactose. Microb Biotechnol. 2017;10(2):492–501.
pubmed: 27910262
doi: 10.1111/1751-7915.12458
Jantama K, Haupt MJ, Svoronos SA, Zhang XL, Moore JC, Shanmugam KT, Ingram LO. Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate. Biotechnol Bioeng. 2008;99(5):1140–53.
pubmed: 17972330
doi: 10.1002/bit.21694
Agren R, Otero JM, Nielsen J. Genome-scale modeling enables metabolic engineering of Saccharomyces cerevisiae for succinic acid production. J Ind Microbiol Biotechnol. 2013;40(7):735–47.
pubmed: 23608777
doi: 10.1007/s10295-013-1269-3
Franco-Duarte R, Bessa D, Gonçalves F, Martins R, Silva-Ferreira AC, Schuller D, Sampaio P, Pais C. Genomic and transcriptomic analysis of isolates with focus in succinic acid production. FEMS Yeast Res. 2017; 17(6).
Ito Y, Hirasawa T, Shimizu H. Metabolic engineering of Saccharomyces cerevisiae to improve succinic acid production based on metabolic profiling. Biosci Biotechnol Biochem. 2014;78(1):151–9.
pubmed: 25036498
doi: 10.1080/09168451.2014.877816
Yan DJ, Wang CX, Zhou JM, Liu YL, Yang MH, Xing JM. Construction of reductive pathway in Saccharomyces cerevisiae for effective succinic acid fermentation at low pH value. Bioresour Technol. 2014;156:232–9.
pubmed: 24508660
doi: 10.1016/j.biortech.2014.01.053
Xiberras J, Klein M, Hulster ED, Mans R, Nevoigt E. Engineering Saccharomyces cerevisiae for succinic acid production from glycerol and carbon dioxide. Front Bioeng Biotechnol. 2020;8:566.
pubmed: 32671027
pmcid: 7332542
doi: 10.3389/fbioe.2020.00566
Malubhoy Z, Bahia FM, de Valk SC, de Hulster E, Rendulic T, Ortiz JPR, Xiberras J, Klein M, Mans R, Nevoigt E. Carbon dioxide fixation via production of succinic acid from glycerol in engineered Saccharomyces cerevisiae. Microb Cell Fact. 2022; 21(1).
Rendulic T, Bahia FM, Soares-Silva I, Nevoigt E, Casal M. The dicarboxylate transporters from the AceTr family and Dct-02 oppositely affect succinic acid production in S. Cerevisiae. J Fungi. 2022; 8(8).
Van De Graaf MJ, Valianpoer F, Fiey G, Delattre L, EAM S. Process for the crystallization of succinic acid. US Patent 2015, US20150057425A1.
Wang G, Tan L, Sun ZY, Gou ZX, Tang YQ, Kida K. Production of bioethanol from rice straw by simultaneous saccharification and fermentation of whole pretreated slurry using Saccharomyces cerevisiae KF-7. Environ Prog Sustain. 2015;34(2):582–8.
doi: 10.1002/ep.11992
Kida K, Kume K, Morimura S, Sonoda Y. Repeated-batch fermentation process using a thermotolerant flocculating yeast constructed by protoplast fusion. J Ferment Bioeng. 1992;74(3):169–73.
doi: 10.1016/0922-338X(92)90078-9
Mans R, van Rossum HM, Wijsman M, Backx A, Kuijpers NGA, van den Broek M, Daran-Lapujade P, Pronk JT, van Maris AJA, Daran JMG. CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res. 2015; 15(2).
Zeng WY, Tang YQ, Gou M, Xia ZY, Kida K. Transcriptomes of a xylose-utilizing industrial flocculating Saccharomyces cerevisiae strain cultured in media containing different sugar sources. AMB Express. 2016;6(1):51.
pubmed: 27485516
pmcid: 4970999
doi: 10.1186/s13568-016-0223-y
Gibson DG. Oligonucleotide assembly in yeast to produce synthetic DNA fragments. Methods Mol Biol. 2012;852:11–21.
pubmed: 22328422
doi: 10.1007/978-1-61779-564-0_2
Sibirny AA. Yeast peroxisomes: structure, functions and biotechnological opportunities. FEMS Yeast Res. 2016; 16(4).
Strijbis K, Distel B. Intracellular acetyl unit transport in fungal carbon metabolism. Eukaryot Cell. 2010;9(12):1809–15.
pubmed: 20889721
pmcid: 3008284
doi: 10.1128/EC.00172-10
Fahien LA, MacDonald MJ. The succinate mechanism of insulin release. Diabetes. 2002;51(9):2669–76.
pubmed: 12196457
doi: 10.2337/diabetes.51.9.2669
Kunze M, Pracharoenwattana I, Smith SM, Hartig A. A central role for the peroxisomal membrane in glyoxylate cycle function. Biochim Biophys Acta. 2006;1763(12):1441–52.
pubmed: 17055076
doi: 10.1016/j.bbamcr.2006.09.009
Chew SY, Chee WJY, Than LTL. The glyoxylate cycle and alternative carbon metabolism as metabolic adaptation strategies of Candida Glabrata: perspectives from Candida albicans and Saccharomyces cerevisiae. J Biomed Sci. 2019; 26.
Cai L, Tu BP. Driving the cell cycle through metabolism. Annu Rev Cell Dev Biol. 2012;28:59–87.
pubmed: 22578140
doi: 10.1146/annurev-cellbio-092910-154010
Xiao W, Wang RS, Handy DE, Loscalzo J. NAD(H) and NADP(H) redox couples and cellular energy metabolism. Antioxid Redox Signal. 2018;28(3):251–72.
pubmed: 28648096
pmcid: 5737637
doi: 10.1089/ars.2017.7216
Kruger A, Gruning NM, Wamelink MMC, Kerick M, Kirpy A, Parkhomchuk D, Bluemlein K, Schweiger MR, Soldatov A, Lehrach H, et al. The pentose phosphate pathway is a metabolic redox sensor and regulates transcription during the antioxidant response. Antioxid Redox Signal. 2011;15(2):311–24.
pubmed: 21348809
doi: 10.1089/ars.2010.3797
Gruning NM, Lehrach H, Ralser M. Regulatory crosstalk of the metabolic network. Trends Biochem Sci. 2010;35(4):220–7.
pubmed: 20060301
doi: 10.1016/j.tibs.2009.12.001
Andersson R, Eisele-Burger AM, Hanzen S, Vielfort K, Oling D, Eisele F, Johansson G, Gustafsson T, Kvint K, Nystrom T. Differential role of cytosolic Hsp70s in longevity assurance and protein quality control. PLoS Genet. 2021; 17(1).
Amm I, Sommer T, Wolf DH. Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim Biophys Acta. 2014;1843(1):182–96.
pubmed: 23850760
doi: 10.1016/j.bbamcr.2013.06.031
Morrissette VA, Rolfes RJ. The intersection between stress responses and inositol pyrophosphates in Saccharomyces cerevisiae. Curr Genet. 2020;66(5):901–10.
pubmed: 32322930
doi: 10.1007/s00294-020-01078-8
Yoshida M, Kato S, Fukuda S, Izawa S. Acquired resistance to severe ethanol stress in Saccharomyces cerevisiae protein quality control. Appl Environ Microbiol. 2021; 87(6).
Brush GS, Najor NA, Dombkowski AA, Cukovic D, Sawarynski KE. Yeast IME2 functions early in meiosis upstream of cell cycle-regulated SBF and MBF targets. PLoS ONE. 2012; 7(2).
Zhang K, Wu XC, Zheng DQ, Petes TD. Effects of temperature on the meiotic recombination landscape of the yeast Saccharomyces cerevisiae. mBio. 2017; 8(6).
Wang HT, Frackman S, Kowalisyn J, Esposito RE, Elder R. Developmental regulation of SPO13, a gene required for separation of homologous chromosomes at meiosis I. Mol Cell Biol. 1987;7(4):1425–35.
pubmed: 3299047
pmcid: 365230
Zeng WY, Tang YQ, Gou M, Sun ZY, Xia ZY, Kida K. Comparative transcriptomes reveal novel evolutionary strategies adopted by Saccharomyces cerevisiae with improved xylose utilization capability. Appl Microbiol Biotechnol. 2017;101(4):1753–67.
pubmed: 28004152
doi: 10.1007/s00253-016-8046-y
Perli T, Wronska AK, Ortiz-Merino RA, Pronk JT, Daran JM. Vitamin requirements and biosynthesis in Saccharomyces cerevisiae. Yeast. 2020;37(4):283–304.
pubmed: 31972058
doi: 10.1002/yea.3461
Mojzita D, Hohmann S. Pdc2 coordinates expression of the THI regulon in the yeast Saccharomyces cerevisiae. Mol Genet Genomics. 2006;276(2):147–61.
pubmed: 16850348
doi: 10.1007/s00438-006-0130-z
Labuschagne PWJ, Divol B. Thiamine: a key nutrient for yeasts during wine alcoholic fermentation. Appl Microbiol Biotechnol. 2021;105(3):953–73.
pubmed: 33404836
doi: 10.1007/s00253-020-11080-2
Rodriguez-Navarro S, Llorente B, Rodriguez-Manzaneque MT, Ramne A, Uber G, Marchesan D, Dujon B, Herrero E, Sunnerhagen P, Perez-Ortin JE. Functional analysis of yeast gene families involved in metabolism of vitamins B1 and B6. Yeast. 2002;19(14):1261–76.
pubmed: 12271461
doi: 10.1002/yea.916
Walvekar AS, Laxman S. Methionine at the heart of anabolism and signaling: perspectives from budding yeast. Front Microbiol. 2019; 10.
Walvekar AS, Srinivasan R, Gupta R, Laxman S. Methionine coordinates a hierarchically organized anabolic program enabling proliferation. Mol Biol Cell. 2018;29(26):3183–200.
pubmed: 30354837
pmcid: 6340205
doi: 10.1091/mbc.E18-08-0515
Zhang MM, Xiong L, Tang YJ, Mehmood MA, Zhao ZK, Bai FW, Zhao XQ. Enhanced acetic acid stress tolerance and ethanol production in Saccharomyces cerevisiae by modulating expression of the de novo purine biosynthesis genes. Biotechnol Biofuels. 2019; 12.
Avrahami-Moyal L, Braun S, Engelberg D. Overexpression of PDE2 or SSD1-V in Saccharomyces cerevisiae W303-1A strain renders it ethanol-tolerant. FEMS Yeast Res. 2012;12(4):447–55.
pubmed: 22380741
doi: 10.1111/j.1567-1364.2012.00795.x
Thevelein JM, de Winde JH. Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1999;33(5):904–18.
pubmed: 10476026
doi: 10.1046/j.1365-2958.1999.01538.x
Nishida N, Jing DY, Kuroda K, Ueda M. Activation of signaling pathways related to cell wall integrity and multidrug resistance by organic solvent in Saccharomyces cerevisiae. Curr Genet. 2014;60(3):149–62.
pubmed: 24378717
doi: 10.1007/s00294-013-0419-5
Liu ZL, Wang X, Weber SA. Tolerant industrial yeast Saccharomyces cerevisiae posses a more robust cell wall integrity signaling pathway against 2-furaldehyde and 5-(hydroxymethyl)-2-furaldehyde. J Biotechnol. 2018;276:15–24.
pubmed: 29665400
doi: 10.1016/j.jbiotec.2018.04.002
Harris A, Wagner M, Du DJ, Raschka S, Nentwig LM, Gohlke H, Smits SHJ, Luisi B, Schmitt L. Structure and efflux mechanism of the yeast pleiotropic drug resistance transporter Pdr5. Nat Commun. 2021; 12(1).
Nygard Y, Mojzita D, Toivari M, Penttila M, Wiebe MG, Ruohonen L. The diverse role of Pdr12 in resistance to weak organic acids. Yeast. 2014;31(6):219–32.
pubmed: 24691985
doi: 10.1002/yea.3011
Abe F. Induction of DAN/TIR yeast cell wall mannoprotein genes in response to high hydrostatic pressure and low temperature. FEBS Lett. 2007;581(25):4993–8.
pubmed: 17910955
doi: 10.1016/j.febslet.2007.09.039
Negoro H, Kotaka A, Matsumura K, Tsutsumi H, Hata Y. Enhancement of malate-production and increase in sensitivity to dimethyl succinate by mutation of the VID24 gene in Saccharomyces cerevisiae. J Biosci Bioeng. 2016;121(6):665–71.
pubmed: 26983942
doi: 10.1016/j.jbiosc.2015.11.012
Li B, Wang L, Wu YJ, Xia ZY, Yang BX, Tang YQ. Improving acetic acid and furfural resistance of xylose-fermenting Saccharomyces cerevisiae strains by regulating novel transcription factors revealed via comparative transcriptomic analysis. Appl Environ Microbiol. 2021; 87(10).
Hernandez-Elvira M, Martinez-Gomez R, Dominguez-Martin E, Mendez A, Kawasaki L, Ongay-Larios L, Coria R. Tunicamycin sensitivity-suppression by high gene dosage reveals new functions of the yeast Hog1 MAP kinase. Cells. 2019; 8(7).
Piper PW, Ortiz-Calderon C, Holyoak C, Coote P, Cole M. Hsp30, the integral plasma membrane heat shock protein of Saccharomyces cerevisiae, is a stress-inducible regulator of plasma membrane H(+)-ATPase. Cell Stress Chaperones. 1997;2(1):12–24.
pubmed: 9250391
pmcid: 312976
doi: 10.1379/1466-1268(1997)002<0012:HTIPMH>2.3.CO;2
Meena RC, Thakur S, Chakrabarti A. Regulation of Saccharomyces cerevisiae plasma membrane H(+)-ATPase (Pma1) by dextrose and Hsp30 during exposure to thermal stress. Indian J Microbiol. 2011;51(2):153–8.
pubmed: 22654157
pmcid: 3209896
doi: 10.1007/s12088-011-0137-y
Tulha J, Lima A, Lucas C, Ferreira C. Saccharomyces cerevisiae glycerol/H + symporter Stl1p is essential for cold/near-freeze and freeze stress adaptation. A simple recipe with high biotechnological potential is given. Microb Cell Fact. 2010;9:82.
pubmed: 21047428
pmcid: 2989305
doi: 10.1186/1475-2859-9-82
Tenreiro S, Nunes PA, Viegas CA, Neves MS, Teixeira MC, Cabral MG, Sa-Correia I. AQR1 gene (ORF YNL065w) encodes a plasma membrane transporter of the major facilitator superfamily that confers resistance to short-chain monocarboxylic acids and quinidine in Saccharomyces cerevisiae. Biochem Biophys Res Commun. 2002;292(3):741–8.
pubmed: 11922628
doi: 10.1006/bbrc.2002.6703
Kwon YD, Kim S, Lee SY, Kim P. Long-term continuous adaptation of Escherichia coli to high succinate stress and transcriptome analysis of the tolerant strain. J Biosci Bioeng. 2011;111(1):26–30.
pubmed: 20829106
doi: 10.1016/j.jbiosc.2010.08.007
Ungelenk S, Moayed F, Ho CT, Grousl T, Scharf A, Mashaghi A, Tans S, Mayer MP, Mogk A, Bukau B. Small heat shock proteins sequester misfolding proteins in near-native conformation for cellular protection and efficient refolding. Nat Commun. 2016;7:13673.
pubmed: 27901028
pmcid: 5141385
doi: 10.1038/ncomms13673
Lytras G, Zacharioudakis I, Tzamarias D. Asymmetric inheritance of the yeast chaperone Hsp26p and its functional consequences. Biochem Biophys Res Commun. 2017;491(4):1055–61.
pubmed: 28780354
doi: 10.1016/j.bbrc.2017.08.009
Wang J, Pareja KA, Kaiser CA, Sevier CS. Redox signaling via the molecular chaperone BiP protects cells against endoplasmic reticulum-derived oxidative stress. Elife. 2014; 3.
Verghese J, Abrams J, Wang YY, Morano KA. Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev. 2012;76(2):115–58.
pubmed: 22688810
pmcid: 3372250
doi: 10.1128/MMBR.05018-11
Campion R, Bloxam L, Burrow K, Brownridge PJ, Pentland DR, Thomas P, Gourlay CW, Eyers CE, Barclay JW, Morgan A. Proteomic analysis of dietary restriction in yeast reveals a role for Hsp26 in replicative lifespan extension. Biochem J. 2021;478(24):4153–67.
pubmed: 34661239
doi: 10.1042/BCJ20210432
de Nobel H, Lawrie L, Brul S, Klis F, Davis M, Alloush H, Coote P. Parallel and comparative analysis of the proteome and transcriptome of sorbic acid-stressed Saccharomyces cerevisiae. Yeast. 2001;18(15):1413–28.
pubmed: 11746603
doi: 10.1002/yea.793
Lawrence CL, Botting CH, Antrobus R, Coote PJ. Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol. 2004;24(8):3307–23.
pubmed: 15060153
pmcid: 381676
doi: 10.1128/MCB.24.8.3307-3323.2004
Feng X, Zhao H. Investigating host dependence of xylose utilization in recombinant Saccharomyces cerevisiae strains using RNA-seq analysis. Biotechnol Biofuels. 2013;6(1):96.
pubmed: 23830104
pmcid: 3706274
doi: 10.1186/1754-6834-6-96
Sardi M, Rovinskiy N, Zhang Y, Gasch AP. Leveraging genetic-background effects in Saccharomyces cerevisiae to improve lignocellulosic hydrolysate tolerance. Appl Environ Microbiol. 2016;82(19):5838–49.
pubmed: 27451446
pmcid: 5038035
doi: 10.1128/AEM.01603-16
Ndukwe JK, Aliyu GO, Onwosi CO, Chukwu KO, Ezugworie FN. Mechanisms of weak acid-induced stress tolerance in yeasts: prospects for improved bioethanol production from lignocellulosic biomass. Process Biochem. 2020;90:118–30.
doi: 10.1016/j.procbio.2019.11.009
Mira NP, Teixeira MC, Sa-Correia I. Adaptive response and tolerance to weak acids in Saccharomyces cerevisiae: a genome-wide view. OMICS. 2010;14(5):525–40.
pubmed: 20955006
pmcid: 3129613
doi: 10.1089/omi.2010.0072
Ribeiro RA, Bourbon-Melo N, Sa-Correia I. The cell wall and the response and tolerance to stresses of biotechnological relevance in yeasts. Front Microbiol. 2022; 13.
Zeng L, Huang J, Feng P, Zhao X, Si Z, Long X, Cheng Q, Yi Y. Transcriptomic analysis of formic acid stress response in Saccharomyces cerevisiae. World J Microbiol Biotechnol. 2022;38(2):34.
pubmed: 34989900
doi: 10.1007/s11274-021-03222-z
Li B, Xie C, Yang B, Gou M, Xia Z, Sun Z, Tang Y. The response mechanisms of industrial Saccharomyces cerevisiae to acetic acid and formic acid during mixed glucose and xylose fermentation. Process Biochem. 2020;91:319–29.
doi: 10.1016/j.procbio.2020.01.002
Kawazoe N, Kimata Y, Izawa S. Acetic acid causes endoplasmic reticulum stress and induces the unfolded protein response in Saccharomyces cerevisiae. Front Microbiol. 2017;8:1192.
pubmed: 28702017
pmcid: 5487434
doi: 10.3389/fmicb.2017.01192
Berterame NM, Porro D, Ami D, Branduardi P. Protein aggregation and membrane lipid modifications under lactic acid stress in wild type and OPI1 deleted Saccharomyces cerevisiae strains. Microb Cell Fact. 2016;15:39.
pubmed: 26887851
pmcid: 4756461
doi: 10.1186/s12934-016-0438-2
Peetermans A, Foulquie-Moreno MR, Thevelein JM. Mechanisms underlying lactic acid tolerance and its influence on lactic acid production in Saccharomyces cerevisiae. Microb Cell. 2021;8(6):111–30.
pubmed: 34055965
pmcid: 8144909
doi: 10.15698/mic2021.06.751
Deng N, Du H, Xu Y. Cooperative response of Pichia kudriavzevii and Saccharomyces cerevisiae to lactic acid stress in Baijiu fermentation. J Agric Food Chem. 2020;68(17):4903–11.
pubmed: 32180399
doi: 10.1021/acs.jafc.9b08052
Lin AP, Anderson SL, Minard KI, McAlister-Henn L. Effects of excess succinate and retrograde control of metabolite accumulation in yeast tricarboxylic cycle mutants. J Biol Chem. 2011;286(39):33737–46.
pubmed: 21841001
pmcid: 3190802
doi: 10.1074/jbc.M111.266890
Terzioğlu E, Alkım C, Arslan M, Balaban BG, Holyavkin C, Kısakesen H, Topaloğlu A, Yılmaz Şahin Ü, Gündüz Işık S, Akman S, et al. Genomic, transcriptomic and physiological analyses of silver-resistant Saccharomyces cerevisiae obtained by evolutionary engineering. Yeast. 2020;37(9–10):413–26.
pubmed: 33464648
doi: 10.1002/yea.3514
Holyavkin C, Turanli-Yildiz B, Yilmaz Ü, Alkim C, Arslan M, Topaloglu A, Kisakesen HI, de Billerbeck G, François JM, Çakar ZP. Genomic, transcriptomic, and metabolic characterization of 2-Phenylethanol-resistant obtained by evolutionary engineering. Front Microbiol. 2023; 14.
Sürmeli Y, Holyavkin C, Topaloglu A, Arslan M, Kisakesen HI, Çakar ZP. Evolutionary engineering and molecular characterization of a caffeine-resistant strain. World J Microb Biot. 2019; 35(12).
Kocaefe-Özsen N, Yilmaz B, Alkim C, Arslan M, Topaloglu A, Kisakesen HL, Gulsev E, Cakar ZP. Physiological and molecular characterization of an oxidative stress-resistant strain obtained by evolutionary engineering. Front Microbiol. 2022; 13.