Abstract
Objectives
To improve tolerance to acetic acid that is present in lignocellulosic hydrolysates and affects bioethanol production by Saccharomyces cerevisiae.
Results
Saccharomyces cerevisiae strains with improved tolerance to acetic acid were obtained through deletion of the JJJ1 gene. The lag phase of the JJJ1 deletion mutant BYΔJJJ1 was ~16 h shorter than that of the parent strain, BY4741, when the fermentation medium contained 4.5 g acetic acid/l. Additionally, the specific ethanol production rate of BYΔJJJ1 was increased (0.057 g/g h) compared to that of the parent strain (0.051 g/g h). Comparative transcription and physiological analyses revealed higher long chain fatty acid, trehalose, and catalase contents might be critical factors responsible for the acetic acid resistance of JJJ1 knockout strains.
Conclusions
JJJ1 deletion improves acetic acid tolerance and ethanol fermentation performance of S. cerevisiae.
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References
Alexandre H, Mathieu B, Charpentier C (1996) Alteration in membrane fluidity and lipid composition, and modulation of H+-ATPase activity in Saccharomyces cerevisiae caused by decanoic acid. Microbiology 142:469–475
Brown JA, Sherlock G, Myers CL et al (2006) Global analysis of gene function in yeast by quantitative phenotypic profiling. Mol Syst Biol 2:2006
Demoinet E, Jacquier A, Lutfalla G et al (2007) The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA 13:1570–1581
Ding J, Bierma J, Smith MR et al (2013) Acetic acid inhibits nutrient uptake in Saccharomyces cerevisiae: auxotrophy confounds the use of yeast deletion libraries for strain improvement. Appl Microbiol Biotechnol 97:7405–7416
Eleutherio E, Panek A, De Mesquita JF et al (2015) Revisiting yeast trehalose metabolism. Curr Genet 61:263–274
Giannattasio S, Guaragnella N, Corte-Real M et al (2005) Acid stress adaptation protects Saccharomyces cerevisiae from acetic acid-induced programmed cell death. Gene 354:93–98
Guaragnella N, Bobba A, Passarella S et al (2010) Yeast acetic acid-induced programmed cell death can occur without cytochrome c release which requires metacaspase YCA1. FEBS Lett 584:224–228
Gueldener U, Heinisch J, Koehler GJ et al (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acid Res 30:e23
Holyoak CD, Stratford M, McMullin Z et al (1996) Activity of the plasma membrane H(+)-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl Environ Microbiol 62:3158–3164
Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511–1527
Lindahl L, Genheden S, Eriksson LA et al (2015) Sphingolipids contribute to acetic acid resistance in Zygosaccharomyces bailii. Biotechnol Bioengdoi. doi:10.1002/bit.25845
Lindberg L, Santos AX, Riezman H et al (2013) Lipidomic profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii reveals critical changes in lipid composition in response to acetic acid stress. PloS One 8:e73936
Liu X, Zhang X, Zhang Z (2014) Point mutation of H3/H4 histones affects acetic acid tolerance in Saccharomyces cerevisiae. J Biotechnol 187:116–123
Ma C, Wei X, Sun C et al (2015) Improvement of acetic acid tolerance of Saccharomyces cerevisiae using a zinc-finger-based artificial transcription factor and identification of novel genes involved in acetic acid tolerance. Appl Microbiol Biotechnol 99:2441–2449
Martins LH, Rabelo SC, da Costa AC (2015) Effects of the pretreatment method on high solids enzymatic hydrolysis and ethanol fermentation of the cellulosic fraction of sugarcane bagasse. Bioresour Technol 191:312–321
Meyer AE, Hung NJ, Yang P et al (2007) The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis. Proc Natl Acad Sci USA 104:1558–1563
Mira NP, Henriques SF, Keller G et al (2011) Identification of a DNA-binding site for the transcription factor Haa1, required for Saccharomyces cerevisiae response to acetic acid stress. Nucleic Acid Res 39:6896–6907
Mollapour M, Piper PW (2007) Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. Mol Cell Biol 27:6446–6456
Palmqvist E, Hahn-Hagerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33
Qureshi AS, Zhang J, Bao J (2015) High ethanol fermentation performance of the dry dilute acid pretreated corn stover by an evolutionarily adapted Saccharomyces cerevisiae strain. Bioresour Technol 189:399–404
Tanaka K, Ishii Y, Ogawa J et al (2012) Enhancement of acetic acid tolerance in Saccharomyces cerevisiae by overexpression of the HAA1 gene, encoding a transcriptional activator. Appl Environ Microbiol 78:8161–8163
Tao X, Zheng D, Liu T et al (2012) A novel strategy to construct yeast Saccharomyces cerevisiae strains for very high gravity fermentation. PloS One 7:e31235
Walsh P, Bursac D, Law YC et al (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5:567–571
Woolford JL Jr, Baserga SJ (2013) Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics 195:643–681
Yoshiyama Y, Tanaka K, Yoshiyama K et al (2015) Trehalose accumulation enhances tolerance of Saccharomyces cerevisiae to acetic acid. J Biosci Bioeng 119:172–175
Zhang JG, Liu XY, He XP et al (2011) Improvement of acetic acid tolerance and fermentation performance of Saccharomyces cerevisiae by disruption of the FPS1 aquaglyceroporin gene. Biotechnol Lett 33:277–284
Zheng DQ, Wu XC, Tao XL et al (2011a) Screening and construction of Saccharomyces cerevisiae strains with improved multi-tolerance and bioethanol fermentation performance. Bioresour Technol 102:3020–3027
Zheng DQ, Wu XC, Wang PM et al (2011b) Drug resistance marker-aided genome shuffling to improve acetic acid tolerance in Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 38:415–422
Zheng DQ, Wang PM, Chen J et al (2012) Genome sequencing and genetic breeding of a bioethanol Saccharomyces cerevisiae strain YJS329. BMC Genom 13:479
Zheng DQ, Liu TZ, Chen J et al (2013) Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Appl Microbiol Biotechnol 97:2067–2076
Acknowledgments
This work was financially supported by the National Natural Science Foundation of China (31370132 and 31401058) and by the State Key Laboratory of Motor Vehicle Biofuels Technology of China.
Supporting information
Supplementary Table 1—Primers used for genetic manipulations.
Supplementary Table 2—Primers used in qRT-PCR.
Supplementary Figure 1—(A) Expression of JJJ1 in BYΔJJJ1 restores the phenotypic change (improvement of the fermentation rate) conferred by JJJ1 deletion in S. cerevisiae.
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Xuechang Wu and Lijie Zhang have contributed equally to this work.
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Wu, X., Zhang, L., Jin, X. et al. Deletion of JJJ1 improves acetic acid tolerance and bioethanol fermentation performance of Saccharomyces cerevisiae strains. Biotechnol Lett 38, 1097–1106 (2016). https://doi.org/10.1007/s10529-016-2085-4
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DOI: https://doi.org/10.1007/s10529-016-2085-4