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Applied Microbiology and Biotechnology

, Volume 103, Issue 1, pp 159–175 | Cite as

Molecular and physiological basis of Saccharomyces cerevisiae tolerance to adverse lignocellulose-based process conditions

  • Joana T. Cunha
  • Aloia Romaní
  • Carlos E. Costa
  • Isabel Sá-Correia
  • Lucília DominguesEmail author
Mini-Review
  • 327 Downloads

Abstract

Lignocellulose-based biorefineries have been gaining increasing attention to substitute current petroleum-based refineries. Biomass processing requires a pretreatment step to break lignocellulosic biomass recalcitrant structure, which results in the release of a broad range of microbial inhibitors, mainly weak acids, furans, and phenolic compounds. Saccharomyces cerevisiae is the most commonly used organism for ethanol production; however, it can be severely distressed by these lignocellulose-derived inhibitors, in addition to other challenging conditions, such as pentose sugar utilization and the high temperatures required for an efficient simultaneous saccharification and fermentation step. Therefore, a better understanding of the yeast response and adaptation towards the presence of these multiple stresses is of crucial importance to design strategies to improve yeast robustness and bioconversion capacity from lignocellulosic biomass. This review includes an overview of the main inhibitors derived from diverse raw material resultants from different biomass pretreatments, and describes the main mechanisms of yeast response to their presence, as well as to the presence of stresses imposed by xylose utilization and high-temperature conditions, with a special emphasis on the synergistic effect of multiple inhibitors/stressors. Furthermore, successful cases of tolerance improvement of S. cerevisiae are highlighted, in particular those associated with other process-related physiologically relevant conditions. Decoding the overall yeast response mechanisms will pave the way for the integrated development of sustainable yeast cell–based biorefineries.

Keywords

Lignocellulosic biomass Inhibitory compounds Stress response mechanisms S. cerevisiae Metabolic engineering 

Notes

Funding

This study was supported by the Portuguese Foundation for Science and Technology (FCT) by the strategic funding of UID/BIO/04469/2013 unit, MIT Portugal Program (Ph.D. grant PD/BD/128247/2016 to Joana T. Cunha), Ph.D. grant SFRH/BD/130739/2017 to Carlos E. Costa, COMPETE 2020 (POCI-01-0145-FEDER-006684), BioTecNorte operation (NORTE-01-0145-FEDER-000004), YeasTempTation (ERA-IB-2-6/0001/2014), and MultiBiorefinery project (POCI-01-0145-FEDER-016403). Funding by the Institute for Bioengineering and Biosciences (IBB) from FCT (UID/BIO/04565/2013) and from Programa Operacional Regional de Lisboa 2020 (Project N. 007317) was also received.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abbott DA, Knijnenburg TA, de Poorter LMI, Reinders MJT, Pronk JT, van Maris AJA (2007) Generic and specific transcriptional responses to different weak organic acids in anaerobic chemostat cultures of Saccharomyces cerevisiae. FEMS Yeast Res 7(6):819–833.  https://doi.org/10.1111/j.1567-1364.2007.00242.x CrossRefPubMedGoogle Scholar
  2. Adeboye PT, Bettiga M, Olsson L (2014) The chemical nature of phenolic compounds determines their toxicity and induces distinct physiological responses in Saccharomyces cerevisiae in lignocellulose hydrolysates. AMB Express 4:46–46.  https://doi.org/10.1186/s13568-014-0046-7 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Adeboye PT, Bettiga M, Aldaeus F, Larsson PT, Olsson L (2015) Catabolism of coniferyl aldehyde, ferulic acid and p-coumaric acid by Saccharomyces cerevisiae yields less toxic products. Microb Cell Factories 14:149.  https://doi.org/10.1186/s12934-015-0338-x CrossRefGoogle Scholar
  4. Adeboye PT, Bettiga M, Olsson L (2017) ALD5, PAD1, ATF1 and ATF2 facilitate the catabolism of coniferyl aldehyde, ferulic acid and p-coumaric acid in Saccharomyces cerevisiae. Sci Rep 7:42635.  https://doi.org/10.1038/srep42635 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Allen SA, Clark W, McCaffery JM, Cai Z, Lanctot A, Slininger PJ, Liu ZL, Gorsich SW (2010) Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol Biofuels 3:2.  https://doi.org/10.1186/1754-6834-3-2 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Alriksson B, Horváth IS, Jönsson L (2010) Overexpression of Saccharomyces cerevisiae transcription factor and multidrug resistance genes conveys enhanced resistance to lignocellulose-derived fermentation inhibitors. Process Biochem 45(2):264–271.  https://doi.org/10.1016/j.procbio.2009.09.016 CrossRefGoogle Scholar
  7. Alvarez-Peral FJ, Zaragoza O, Pedreno Y, Argüelles J-C (2002) Protective role of trehalose during severe oxidative stress caused by hydrogen peroxide and the adaptive oxidative stress response in Candida albicans. Microbiol 148(8):2599–2606.  https://doi.org/10.1099/00221287-148-8-2599 CrossRefGoogle Scholar
  8. Alvira P, Negro MJ, Ballesteros M (2011) Effect of endoxylanase and α-L-arabinofuranosidase supplementation on the enzymatic hydrolysis of steam exploded wheat straw. Bioresour Technol 102(6):4552–4558.  https://doi.org/10.1016/j.biortech.2010.12.112 CrossRefPubMedGoogle Scholar
  9. Ask M, Bettiga M, Mapelli V, Olsson L (2013) The influence of HMF and furfural on redox-balance and energy-state of xylose-utilizing Saccharomyces cerevisiae. Biotechnol Biofuels 6(1):22.  https://doi.org/10.1186/1754-6834-6-22 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bellissimi E, van Dijken JP, Pronk JT, van Maris AJ (2009) Effects of acetic acid on the kinetics of xylose fermentation by an engineered, xylose-isomerase-based Saccharomyces cerevisiae strain. FEMS Yeast Res 9(3):358–364.  https://doi.org/10.1111/j.1567-1364.2009.00487.x CrossRefPubMedGoogle Scholar
  11. Brandberg T, FranzéN CJ, Gustafsson L (2004) The fermentation performance of nine strains of Saccharomyces cerevisiae in batch and fed-batch cultures in dilute-acid wood hydrolysate. J Biosci Bioeng 98:122–125.  https://doi.org/10.1016/S1389-1723(04)70252-2 CrossRefPubMedGoogle Scholar
  12. Campos FM, Couto JA, Figueiredo AR, Toth IV, Rangel AO, Hogg TA (2009) Cell membrane damage induced by phenolic acids on wine lactic acid bacteria. Int J Food Microbiol 135(2):144–151.  https://doi.org/10.1016/j.ijfoodmicro.2009.07.031 CrossRefPubMedGoogle Scholar
  13. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA (2001) Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 12(2):323–337.  https://doi.org/10.1091/mbc.12.2.323 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Celton M, Goelzer A, Camarasa C, Fromion V, Dequin S (2012) A constraint-based model analysis of the metabolic consequences of increased NADPH oxidation in Saccharomyces cerevisiae. Metab Eng 14:366–379.  https://doi.org/10.1016/j.ymben.2012.03.008 CrossRefPubMedGoogle Scholar
  15. Costa CE, Romani A, Cunha JT, Johansson B, Domingues L (2017) Integrated approach for selecting efficient Saccharomyces cerevisiae for industrial lignocellulosic fermentations: importance of yeast chassis linked to process conditions. Bioresour Technol 227:24–34.  https://doi.org/10.1016/j.biortech.2016.12.016 CrossRefPubMedGoogle Scholar
  16. Cunha JT, Aguiar TQ, Romani A, Oliveira C, Domingues L (2015) Contribution of PRS3, RPB4 and ZWF1 to the resistance of industrial Saccharomyces cerevisiae CCUG53310 and PE-2 strains to lignocellulosic hydrolysate-derived inhibitors. Bioresour Technol 191:7–16.  https://doi.org/10.1016/j.biortech.2015.05.006 CrossRefPubMedGoogle Scholar
  17. Cunha JT, Costa CE, Ferraz L, Romani A, Johansson B, Sa-Correia I, Domingues L (2018) HAA1 and PRS3 overexpression boosts yeast tolerance towards acetic acid improving xylose or glucose consumption: unravelling the underlying mechanisms. Appl Microbiol Biotechnol 102(10):4589–4600.  https://doi.org/10.1007/s00253-018-8955-z CrossRefPubMedGoogle Scholar
  18. Damay J, Boboescu I-Z, Duret X, Lalonde O, Lavoie J-M (2018) A novel hybrid first and second generation hemicellulosic bioethanol production process through steam treatment of dried sorghum biomass. Bioresour Technol 263:103–111.  https://doi.org/10.1016/j.biortech.2018.04.045 CrossRefPubMedGoogle Scholar
  19. Della-Bianca BE, Gombert AK (2013) Stress tolerance and growth physiology of yeast strains from the Brazilian fuel ethanol industry. Antonie Van Leeuwenhoek 104:1083–1095.  https://doi.org/10.1007/s10482-013-0030-2 CrossRefPubMedGoogle Scholar
  20. Demeke MM, Dietz H, Li Y, Foulquié-Moreno MR, Mutturi S, Deprez S, Den Abt T, Bonini BM, Liden G, Dumortier F, Verplaetse A, Boles E, Thevelein JM (2013a) Development of a D-xylose fermenting and inhibitor tolerant industrial Saccharomyces cerevisiae strain with high performance in lignocellulose hydrolysates using metabolic and evolutionary engineering. Biotechnol Biofuels 6(1):89.  https://doi.org/10.1186/1754-6834-6-89 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Demeke MM, Dumortier F, Li Y, Broeckx T, Foulquié-Moreno MR, Thevelein JM (2013b) Combining inhibitor tolerance and D-xylose fermentation in industrial Saccharomyces cerevisiae for efficient lignocellulose-based bioethanol production. Biotechnol Biofuels 6:120–120.  https://doi.org/10.1186/1754-6834-6-120 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Deparis Q, Claes A, Foulquié-Moreno MR, Thevelein JM (2017) Engineering tolerance to industrially relevant stress factors in yeast cell factories. FEMS Yeast Research 17(4).  https://doi.org/10.1093/femsyr/fox036
  23. Ding MZ, Wang X, Yang Y, Yuan YJ (2011) Metabolomic study of interactive effects of phenol, furfural, and acetic acid on Saccharomyces cerevisiae. OMICS 15(10):647–653.  https://doi.org/10.1089/omi.2011.0003 CrossRefPubMedGoogle Scholar
  24. Dominguez E, Romaní A, Domingues L, Garrote G (2017) Evaluation of strategies for second generation bioethanol production from fast growing biomass Paulownia within a biorefinery scheme. Appl Energy 187:777–789.  https://doi.org/10.1016/j.apenergy.2016.11.114 CrossRefGoogle Scholar
  25. Dong Y, Hu J, Fan L, Chen Q (2017) RNA-Seq-based transcriptomic and metabolomic analysis reveal stress responses and programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Sci Rep 7:42659.  https://doi.org/10.1038/srep42659 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Eisenberg T, Knauer H, Schauer A, Büttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, Fussi H, Deszcz L, Hartl R, Schraml E, Criollo A, Megalou E, Weiskopf D, Laun P, Heeren G, Breitenbach M, Grubeck-Loebenstein B, Herker E, Fahrenkrog B, Fröhlich K-U, Sinner F, Tavernarakis N, Minois N, Kroemer G, Madeo F (2009) Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 11:1305–1314.  https://doi.org/10.1038/ncb1975 CrossRefPubMedGoogle Scholar
  27. Fernandes AR, Mira NP, Vargas RC, Canelhas I, Sá-Correia I (2005) Saccharomyces cerevisiae adaptation to weak acids involves the transcription factor Haa1p and Haa1p-regulated genes. Bioche Biophys Res Commun 337(1):95–103.  https://doi.org/10.1016/j.bbrc.2005.09.010
  28. Foretek D, Wu J, Hopper AK, Boguta M (2016) Control of Saccharomyces cerevisiae pre-tRNA processing by environmental conditions. RNA 22:339–349.  https://doi.org/10.1261/rna.054973.115 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Frohner IE, Gregori C, Anrather D, Roitinger E, Schüller C, Ammerer G, Kuchler K (2010) Weak organic acid stress triggers hyperphosphorylation of the yeast zinc-finger transcription factor War1 and dampens stress adaptation. OMICS 14(5):575–586.  https://doi.org/10.1089/omi.2010.0032 CrossRefPubMedGoogle Scholar
  30. Gao L, Liu Y, Sun H, Li C, Zhao Z, Liu G (2016) Advances in mechanisms and modifications for rendering yeast thermotolerance. J Biosci Bioeng 121(6):599–606.  https://doi.org/10.1016/j.jbiosc.2015.11.002 CrossRefPubMedGoogle Scholar
  31. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11(12):4241–4257.  https://doi.org/10.1091/mbc.11.12.4241 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Giannattasio S, Guaragnella N, Ždralević M, Marra E (2013) Molecular mechanisms of Saccharomyces cerevisiae stress adaptation and programmed cell death in response to acetic acid. Front Microbiol 4:33.  https://doi.org/10.3389/fmicb.2013.00033 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Godinho CP, Prata CS, Pinto SN, Cardoso C, Bandarra NM, Fernandes F, Sá-Correia I (2018) Pdr18 is involved in yeast response to acetic acid stress counteracting the decrease of plasma membrane ergosterol content and order. Sci Rep 8(1):7860.  https://doi.org/10.1038/s41598-018-26128-7 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gomes DG, Guimarães PMR, Pereira FB, Teixeira JA, Domingues L (2012) Plasmid-mediate transfer of FLO-1 into industrial Saccharomyces cerevisiae PE-2 strain creates a strain useful for repeat-batch fermentations involving flocculation-sedimentation. Bioresour Technol 108:162–168.  https://doi.org/10.1016/j.biortech.2011.12.089 CrossRefPubMedGoogle Scholar
  35. Gopinarayanan VE, Nair NU (2018) A semi-synthetic regulon enables rapid growth of yeast on xylose. Nat Commun 9:1233.  https://doi.org/10.1038/s41467-018-03645-7 CrossRefGoogle Scholar
  36. Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD (2006) Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 71(3):339–349.  https://doi.org/10.1007/s00253-005-0142-3 CrossRefPubMedGoogle Scholar
  37. Gregori C, Schuller C, Frohner IE, Ammerer G, Kuchler K (2008) Weak organic acids trigger conformational changes of the yeast transcription factor War1 in vivo to elicit stress adaptation. J Biol Chem 283(37):25752–25764.  https://doi.org/10.1074/jbc.M803095200 CrossRefPubMedGoogle Scholar
  38. Guerreiro JF, Muir A, Ramachandran S, Thorner J, Sa-Correia I (2016) Sphingolipid biosynthesis upregulation by TOR complex 2-Ypk1 signaling during yeast adaptive response to acetic acid stress. Biochem J 473(23):4311–4325.  https://doi.org/10.1042/BCJ20160565 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Guo Z, Olsson L (2014) Physiological response of Saccharomyces cerevisiae to weak acids present in lignocellulosic hydrolysate. FEMS Yeast Res 14(8):1234–1248.  https://doi.org/10.1111/1567-1364.12221 CrossRefPubMedGoogle Scholar
  40. Hasan R, Leroy C, Isnard A-D, Labarre J, Boy-Marcotte E, Toledano MB (2002) The control of the yeast H2O2 response by the Msn2/4 transcription factors. Mol Microbiol 45(1):233–241.  https://doi.org/10.1046/j.1365-2958.2002.03011.x CrossRefPubMedGoogle Scholar
  41. Hasunuma T, Hori Y, Sakamoto T, Ochiai M, Hatanaka H, Kondo A (2014) Development of a GIN11/FRT-based multiple-gene integration technique affording inhibitor-tolerant, hemicellulolytic, xylose-utilizing abilities to industrial Saccharomyces cerevisiae strains for ethanol production from undetoxified lignocellulosic hemicelluloses. Microb Cell Factories 13:145.  https://doi.org/10.1186/s12934-014-0145-9 CrossRefGoogle Scholar
  42. Hawkins GM, Doran-Peterson J (2011) A strain of Saccharomyces cerevisiae evolved for fermentation of lignocellulosic biomass displays improved growth and fermentative ability in high solids concentrations and in the presence of inhibitory compounds. Biotechnol Biofuels 4:49.  https://doi.org/10.1186/1754-6834-4-49 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Heer D, Heine D, Sauer U (2009) Resistance of Saccharomyces cerevisiae to high concentrations of furfural is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol 75(24):7631–7638.  https://doi.org/10.1128/aem.01649-09 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hélène D, Nolwenn D, Moïse P, Monique BF (2000) A large-scale study of Yap1p-dependent genes in normal aerobic and H2O2-stress conditions: the role of Yap1p in cell proliferation control in yeast. Mol Microbiol 36(4):830–845.  https://doi.org/10.1046/j.1365-2958.2000.01845.x CrossRefGoogle Scholar
  45. Henriques SF, Mira NP, Sá-Correia I (2017) Genome-wide search for candidate genes for yeast robustness improvement against formic acid reveals novel susceptibility (Trk1 and positive regulators) and resistance (Haa1-regulon) determinants. Biotechnol Biofuels 10:96.  https://doi.org/10.1186/s13068-017-0781-5 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Herrero E, Ros J, Bellí G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780(11):1217–1235.  https://doi.org/10.1016/j.bbagen.2007.12.004 CrossRefPubMedGoogle Scholar
  47. Higgins VJ, Beckhouse AG, Oliver AD, Rogers PJ, Dawes IW (2003) Yeast genome-wide expression analysis identifies a strong ergosterol and oxidative stress response during the initial stages of an industrial lager fermentation. Appl Environ Microbiol 69(8):4777–4787.  https://doi.org/10.1128/aem.69.8.4777-4787.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Iwaki A, Kawai T, Yamamoto Y, Izawa S (2013a) Biomass conversion inhibitors furfural and 5-hydroxymethylfurfural induce formation of messenger RNP granules and attenuate translation activity in Saccharomyces cerevisiae. Appl Environ Microbiol 79(5):1661–1667.  https://doi.org/10.1128/AEM.02797-12 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Iwaki A, Ohnuki S, Suga Y, Izawa S, Ohya Y (2013b) Vanillin inhibits translation and induces messenger ribonucleoprotein (mRNP) granule formation in Saccharomyces cerevisiae: application and validation of high-content, image-based profiling. PLoS One 8(4):e61748.  https://doi.org/10.1371/journal.pone.0061748 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Jain NK, Roy I (2009) Effect of trehalose on protein structure. Protein Sci 18(1):24–36.  https://doi.org/10.1002/pro.3 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jayakody LN, Turner TL, Yun EJ, Kong II, Liu JJ, Jin YS (2018) Expression of Gre2p improves tolerance of engineered xylose-fermenting Saccharomyces cerevisiae to glycolaldehyde under xylose metabolism. Appl Microbiol Biotechnol 102(18):8121–8133.  https://doi.org/10.1007/s00253-018-9216-x CrossRefPubMedGoogle Scholar
  52. Jesus MS, Romaní A, Genisheva Z, Teixeira JA, Domingues L (2017) Integral valorization of vine pruning residue by sequential autohydrolysis stages. J Clea Prod 168:74–86.  https://doi.org/10.1016/j.jclepro.2017.08.230 CrossRefGoogle Scholar
  53. Jin M, Sarks C, Gunawan C, Bice BD, Simonett SP, Narasimhan RA, Willis LB, Dale BE, Venkatesh B, Sato TK (2013) Phenotypic selection of a wild Saccharomyces cerevisiae strain for simultaneous saccharification and co-fermentation of AFEX™ pretreated corn stover. Biotechnol Biofuels 6:108.  https://doi.org/10.1186/1754-6834-6-108 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Keating JD, Panganiban C, Mansfield SD (2006) Tolerance and adaptation of ethanologenic yeasts to lignocellulosic inhibitory compounds. Biotechnol Bioeng 93(6):1196–1206.  https://doi.org/10.1002/bit.20838 CrossRefPubMedGoogle Scholar
  55. Kelbert M, Romaní A, Coelho E, Pereira FB, Teixeira JA, Domingues L (2015) Lignocellulosic bioethanol production with revalorization of low-cost agroindustrial by-products as nutritional supplements. Ind Crop Prod 64:16–24.  https://doi.org/10.1016/j.indcrop.2014.10.056 CrossRefGoogle Scholar
  56. Kelbert M, Romaní A, Coelho E, Pereira FB, Teixeira JA, Domingues L (2016) Simultaneous saccharification and fermentation of hydrothermal pretreated lignocellulosic biomass: evaluation of process performance under multiple stress conditions. Bioen Res 9:750–762.  https://doi.org/10.1007/s12155-016-9722-6 CrossRefGoogle Scholar
  57. Kim D, Hahn J-S (2013) Roles of the Yap1 transcription factor and antioxidants in Saccharomyces cerevisiae’s tolerance to furfural and 5-hydroxymethylfurfural, which function as thiol-reactive electrophiles generating oxidative stress. Appl Environ Microbiol 79(16):5069–5077.  https://doi.org/10.1128/aem.00643-13 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Kim SR, Xu H, Lesmana A, Kuzmanovic U, Au M, Florencia C, Oh EJ, Zhang G, Kim KH, Jin Y-S (2015) Deletion of PHO13, encoding haloacid dehalogenase type iia phosphatase, results in upregulation of the pentose phosphate pathway in Saccharomyces cerevisiae. Appl Environ Microbiol 81(5):1601–1609.  https://doi.org/10.1128/aem.03474-14 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Kim S-K, Jo J-H, Jin Y-S, Seo J-H (2017a) Enhanced ethanol fermentation by engineered Saccharomyces cerevisiae strains with high spermidine contents. Bioprocess Biosyst Eng 40(5):683–691.  https://doi.org/10.1007/s00449-016-1733-3 CrossRefPubMedGoogle Scholar
  60. Kim SR, Skerker JM, Kong II, Kim H, Maurer MJ, Zhang GC, Peng D, Wei N, Arkin AP, Jin YS (2017b) Metabolic engineering of a haploid strain derived from a triploid industrial yeast for producing cellulosic ethanol. Metab Eng 40:176–185.  https://doi.org/10.1016/j.ymben.2017.02.006 CrossRefPubMedGoogle Scholar
  61. Klinke HB, Olsson L, Thomsen AB, Ahring BK (2003) Potential inhibitors from wet oxidation of wheat straw and their effect on ethanol production of Saccharomyces cerevisiae: wet oxidation and fermentation by yeast. Biotechnol Bioeng 81(6):738–747.  https://doi.org/10.1002/bit.10523 CrossRefPubMedGoogle Scholar
  62. Ko JK, Um Y, Park YC, Seo JH, Kim KH (2015) Compounds inhibiting the bioconversion of hydrothermally pretreated lignocellulose. Appl Microbiol Biotechnol 99(10):4201–4212.  https://doi.org/10.1007/s00253-015-6595-0 CrossRefPubMedGoogle Scholar
  63. Kren A, Mamnun YM, Bauer BE, Schüller C, Wolfger H, Hatzixanthis K, Mollapour M, Gregori C, Piper P, Kuchler K (2003) War1p, a novel transcription factor controlling weak acid stress response in yeast. Mol Cell Biol 23(5):1775–1785.  https://doi.org/10.1128/mcb.23.5.1775-1785.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Kuang Z, Pinglay S, Ji H, Boeke JD (2017) Msn2/4 regulate expression of glycolytic enzymes and control transition from quiescence to growth. eLife 6:e29938.  https://doi.org/10.7554/eLife.29938 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Lane S, Xu H, Oh EJ, Kim H, Lesmana A, Jeong D, Guochang Z, Tsai C-S, Jin Y-S, Kim SR (2018) Glucose repression can be alleviated by reducing glucose phosphorylation rate in Saccharomyces cerevisiae. Sci Rep 8:2613.  https://doi.org/10.1038/s41598-018-20804-4 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Larochelle M, Drouin S, Robert F, Turcotte B (2006) Oxidative stress-activated zinc cluster protein Stb5 has dual activator/repressor functions required for pentose phosphate pathway regulation and NADPH production. Mol Cell Biol 26(17):6690–6701.  https://doi.org/10.1128/mcb.02450-05 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Larsson S, Quintana-Sainz A, Reimann A, Nilvebrant NO, Jonsson LJ (2000) Influence of lignocellulose-derived aromatic compounds on oxygen-limited growth and ethanolic fermentation by Saccharomyces cerevisiae. Appl Biochem Biotechnol 84-86:617–632CrossRefGoogle Scholar
  68. Larsson S, Cassland P, Jönsson LJ (2001) Development of a Saccharomyces cerevisiae strain with enhanced resistance to phenolic fermentation inhibitors in lignocellulose hydrolysates by heterologous expression of laccase. Appl Environ Microbiol 67(3):1163–1170.  https://doi.org/10.1128/aem.67.3.1163-1170.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Lavoie JM, Capek-Menard E, Gauvin H, Chornet E (2010) Production of pulp from Salix vinimalis energy crops using the FIRSST process. Bioresour Technol 101:4940–4946.  https://doi.org/10.1016/j.biortech.2009.09.021 CrossRefPubMedGoogle Scholar
  70. Levin DE (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 69(2):262–291.  https://doi.org/10.1128/MMBR.69.2.262-291.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189(4):1145–1175.  https://doi.org/10.1534/genetics.111.128264 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Lin FM, Qiao B, Yuan YJ (2009) Comparative proteomic analysis of tolerance and adaptation of ethanologenic Saccharomyces cerevisiae to furfural, a lignocellulosic inhibitory compound. Appl Environ Microbiol 75(11):3765–3776.  https://doi.org/10.1128/AEM.02594-08 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Lindberg L, Santos AXS, Riezman H, Olsson L, Bettiga M (2013) Lipidomic profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii reveals critical changes in lipid composition in response to acetic acid stress. PLoS One 8(9):e73936.  https://doi.org/10.1371/journal.pone.0073936 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Liu ZL, Moon J (2009) A novel NADPH-dependent aldehyde reductase gene from Saccharomyces cerevisiae NRRL Y-12632 involved in the detoxification of aldehyde inhibitors derived from lignocellulosic biomass conversion. Gene 446(1):1–10.  https://doi.org/10.1016/j.gene.2009.06.018 CrossRefPubMedGoogle Scholar
  75. Liu ZL, Slininger PJ, Dien BS, Berhow MA, Kurtzman CP, Gorsich SW (2004) Adaptive response of yeasts to furfural and 5-hydroxymethylfurfural and new chemical evidence for HMF conversion to 2,5-bis-hydroxymethylfuran. J Ind Microbiol Biotechnol 31(8):345–352.  https://doi.org/10.1007/s10295-004-0148-3 CrossRefPubMedGoogle Scholar
  76. Liu ZL, Slininger PJ, Gorsich SW (2005) Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 121:451–460.  https://doi.org/10.1385/ABAB:121:1-3:0451 CrossRefPubMedGoogle Scholar
  77. Liu ZL, Moon J, Andersh BJ, Slininger PJ, Weber S (2008) Multiple gene-mediated NAD(P)H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and 5-hydroxymethylfurfural by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 81(4):743–753.  https://doi.org/10.1007/s00253-008-1702-0 CrossRefPubMedGoogle Scholar
  78. Liu ZL, Wang X, Weber SA (2018) Tolerant industrial yeast Saccharomyces cerevisiae posses a more robust cell wall integrity signaling pathway against 2-furaldehyde and 5-(hydroxymethyl)-2-furaldehyde. J Biotechnol 276-277:15–24.  https://doi.org/10.1016/j.jbiotec.2018.04.002 CrossRefPubMedGoogle Scholar
  79. Ma M, Liu ZL (2010) Comparative transcriptome profiling analyses during the lag phase uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as key regulatory genes in genomic adaptation to the lignocellulose derived inhibitor HMF for Saccharomyces cerevisiae. BMC Genomics 11:660–660.  https://doi.org/10.1186/1471-2164-11-660 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Maeta K, Izawa S, Okazaki S, Kuge S, Inoue Y (2004) Activity of the Yap1 transcription factor in Saccharomyces cerevisiae is modulated by methylglyoxal, a metabolite derived from glycolysis. Mol Cell Biol 24(19):8753–8764.  https://doi.org/10.1128/mcb.24.19.8753-8764.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Mensonides FIC, Brul S, Hellingwerf KJ, Bakker BM, Teixeira de Mattos MJ (2014) A kinetic model of catabolic adaptation and protein reprofiling in Saccharomyces cerevisiae during temperature shifts. FEBS J 281(3):825–841.  https://doi.org/10.1111/febs.12649 CrossRefPubMedGoogle Scholar
  82. Mira NP, Becker JD, Sa-Correia I (2010) Genomic expression program involving the Haa1p-regulon in Saccharomyces cerevisiae response to acetic acid. OMICS 14(5):587–601.  https://doi.org/10.1089/omi.2010.0048 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Modenbach AA, Nokes SE (2012) The use of high-solids loadings in biomass pretreatment—a review. Biotechnol Bioeng 109(6):1430–1442.  https://doi.org/10.1002/bit.24464 CrossRefPubMedGoogle Scholar
  84. Morano KA, Grant CM, Moye-Rowley WS (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190:1157–1195.  https://doi.org/10.1534/genetics.111.128033 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Moysés DN, Reis VC, de Almeida JR, de Moraes LM, Torres FA (2016) Xylose fermentation by Saccharomyces cerevisiae: challenges and prospects. Int J Mol Sci 17:207.  https://doi.org/10.3390/ijms17030207 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Nguyen TT, Kitajima S, Izawa S (2014a) Importance of glucose-6-phosphate dehydrogenase (G6PDH) for vanillin tolerance in Saccharomyces cerevisiae. J Biosci Bioeng 118(3):263–269.  https://doi.org/10.1016/j.jbiosc.2014.02.025 CrossRefPubMedGoogle Scholar
  87. Nguyen TTM, Iwaki A, Ohya Y, Izawa S (2014b) Vanillin causes the activation of Yap1 and mitochondrial fragmentation in Saccharomyces cerevisiae. J Biosci Bioeng 117(1):33–38.  https://doi.org/10.1016/j.jbiosc.2013.06.008 CrossRefPubMedGoogle Scholar
  88. Nishida N, Jing D, Kuroda K, Ueda M (2014) Activation of signaling pathways related to cell wall integrity and multidrug resistance by organic solvent in Saccharomyces cerevisiae. Curr Genet 60(3):149–162.  https://doi.org/10.1007/s00294-013-0419-5 CrossRefPubMedGoogle Scholar
  89. Nygård Y, Mojzita D, Toivari M, Penttilä M, Wiebe MG, Ruohonen L (2014) The diverse role of Pdr12 in resistance to weak organic acids. Yeast 31(6):219–232.  https://doi.org/10.1002/yea.3011 CrossRefPubMedGoogle Scholar
  90. Osiro KO, Brink DP, Borgström C, Wasserstrom L, Carlquist M, Gorwa-Grauslund MF (2018) Assessing the effect of d-xylose on the sugar signaling pathways of Saccharomyces cerevisiae in strains engineered for xylose transport and assimilation. FEMS Yeast Res 18(1).  https://doi.org/10.1093/femsyr/fox096
  91. Ouyang X, Tran QT, Goodwin S, Wible RS, Sutter CH, Sutter TR (2011) Yap1 activation by H2O2 or thiol-reactive chemicals elicits distinct adaptive gene responses. Free Radic Biol Med 50(1):1–13.  https://doi.org/10.1016/j.freeradbiomed.2010.10.697 CrossRefPubMedGoogle Scholar
  92. Palma M, Guerreiro JF, Sa-Correia I (2018) Adaptive response and tolerance to acetic acid in Saccharomyces cerevisiae and Zygosaccharomyces bailii: a physiological genomics perspective. Front Microbiol 9:274.  https://doi.org/10.3389/fmicb.2018.00274 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Palmqvist E, Grage H, Meinander NQ, Hahn-Hägerdal B (1999) Main and interaction effects of acetic acid, furfural, and p-hydroxybenzoic acid on growth and ethanol productivity of yeasts. Biotechnol Bioeng 63(1):46–55.  https://doi.org/10.1002/(SICI)10970290(19990405)63:1<46::AID-BIT5>3.0.CO;2-J CrossRefPubMedGoogle Scholar
  94. Pampulha ME, Loureiro-Dias MC (1990) Activity of glycolytic enzymes of Saccharomyces cerevisiae in the presence of acetic acid. Appl Microbiol Biotechnol 34(3):375–380.  https://doi.org/10.1007/bf00170063 CrossRefGoogle Scholar
  95. Pearce AK, Booth IR, Brown AJ (2001) Genetic manipulation of 6-phosphofructo-1-kinase and fructose 2,6-bisphosphate levels affects the extent to which benzoic acid inhibits the growth of Saccharomyces cerevisiae. Microbiol 147:403–410.  https://doi.org/10.1099/00221287-147-2-403 CrossRefGoogle Scholar
  96. Pereira C, Chaves S, Alves S, Salin B, Camougrand N, Manon S, Sousa MJ, Corte-Real M (2010a) Mitochondrial degradation in acetic acid-induced yeast apoptosis: the role of Pep4 and the ADP/ATP carrier. Mol Microbiol 76(6):1398–1410.  https://doi.org/10.1111/j.1365-2958.2010.07122.x CrossRefPubMedGoogle Scholar
  97. Pereira FB, Guimarães PMR, Teixeira JA, Domingues L (2010b) Optimization of low-cost medium for very high gravity ethanol fermentations by Saccharomyces cerevisiae using statistical experimental designs. Bioresour Technol 101:7856–7863.  https://doi.org/10.1016/j.biortech.2010.04.082 CrossRefPubMedGoogle Scholar
  98. Pereira FB, Guimarães PMR, Teixeira JA, Domingues L (2010c) Selection of Saccharomyces cerevisiae strains for efficient very high gravity bio-ethanol fermentation processes. Biotechnol Lett 32:1655–1661.  https://doi.org/10.1007/s10529-010-0330-9 CrossRefPubMedGoogle Scholar
  99. Pereira FB, Guimarães PMR, Gomes DG, Mira NP, Teixeira MC, Sá-Correia I, Domingues L (2011a) Identification of candidate genes for yeast engineering to improve bioethanol production in very-high-gravity and lignocellulosic biomass industrial fermentations. Biotechnol Biofuels 4:57.  https://doi.org/10.1186/1754-6834-4-57 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Pereira FB, Guimarães PMR, Teixeira JA, Domingues L (2011b) Robust industrial Saccharomyces cerevisiae strains for very high gravity bio-ethanol fermentations. J Biosci Bioeng 112:130–136.  https://doi.org/10.1016/j.jbiosc.2011.03.022
  101. Pereira FB, Romaní A, Ruiz HA, Teixeira JA, Domingues L (2014a) Industrial robust yeast isolates with great potential for fermentation of lignocellulosic biomass. Bioresour Technol 161:192–199.  https://doi.org/10.1016/j.biortech.2014.03.043 CrossRefPubMedGoogle Scholar
  102. Pereira FB, Teixeira MC, Mira NP, Sá-Correia I, Domingues L (2014b) Genome-wide screening of Saccharomyces cerevisiae genes required to foster tolerance towards industrial wheat straw hydrolysates. J Ind Microbiol Biotechnol 41:1753–1761.  https://doi.org/10.1007/s10295-014-1519-z
  103. Petitjean M, Teste M-A, François JM, Parrou J-L (2015) Yeast tolerance to various stresses relies on the trehalose-6p synthase (Tps1) protein, not on trehalose. J Biol Chem 290(26):16177–16190.  https://doi.org/10.1074/jbc.M115.653899 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Purwadi R, Brandberg T, Taherzadeh MJ (2007) A possible industrial solution to ferment lignocellulosic hydrolyzate to ethanol: continuous cultivation with flocculating yeast. Int J Mol Sci 8:920–932.  https://doi.org/10.3390/i8090920 CrossRefPubMedCentralGoogle Scholar
  105. Roelants FM, Breslow DK, Muir A, Weissman JS, Thorner J (2011) Protein kinase Ypk1 phosphorylates regulatory proteins Orm1 and Orm2 to control sphingolipid homeostasis in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 108(48):19222–19227.  https://doi.org/10.1073/pnas.1116948108 CrossRefPubMedPubMedCentralGoogle Scholar
  106. Romaní A, Ruíz HA, Pereira FB, Teixeira JA, Domingues L (2014) Integrated approach for effective bioethanol production using whole slurry from autohydrolyzed Eucalyptus globulus wood at high-solid loadings. Fuel 135:482–491.  https://doi.org/10.1016/j.fuel.2014.06.061 CrossRefGoogle Scholar
  107. Romaní A, Pereira F, Johansson B, Domingues L (2015) Metabolic engineering of Saccharomyces cerevisiae ethanol strains PE-2 and CAT-1 for efficient lignocellulosic fermentation. Bioresour Technol 179:150–158.  https://doi.org/10.1016/j.biortech.2014.12.020 CrossRefPubMedGoogle Scholar
  108. Salusjärvi L, Pitkänen JP, Aristidou A, Ruohonen L, Penttilä M (2006) Transcription analysis of recombinant Saccharomyces cerevisiae reveals novel responses to xylose. Appl Biochem Biotechnol 128:237–261.  https://doi.org/10.1385/ABAB:128:3:237 CrossRefPubMedGoogle Scholar
  109. Serrano R (1984) Plasma membrane ATPase of fungi and plants as a novel type of proton pump. Curr Top Cell Reg 23:87–126.  https://doi.org/10.1016/B978-0-12-152823-2.50007-6 CrossRefGoogle Scholar
  110. Simões T, Mira NP, Fernandes AR, Sa-Correia I (2006) The SPI1 gene, encoding a glycosylphosphatidylinositol-anchored cell wall protein, plays a prominent role in the development of yeast resistance to lipophilic weak-acid food preservatives. Appl Environ Microbiol 72(11):7168–7175.  https://doi.org/10.1128/AEM.01476-06 CrossRefPubMedPubMedCentralGoogle Scholar
  111. Subtil T, Boles E (2012) Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnol Biofuels 5:14.  https://doi.org/10.1186/1754-6834-5-14 CrossRefPubMedPubMedCentralGoogle Scholar
  112. Sun Y, Miao Y, Yamane Y, Zhang C, Shokat KM, Takematsu H, Kozutsumi Y, Drubin DG (2012) Orm protein phosphoregulation mediates transient sphingolipid biosynthesis response to heat stress via the Pkh-Ypk and Cdc55-PP2A pathways. Mol Biol Cell 23(12):2388–2398.  https://doi.org/10.1091/mbc.E12-03-0209 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Sundström L, Larsson S, Jönsson LJ (2010) Identification of Saccharomyces cerevisiae genes involved in the resistance to phenolic fermentation inhibitors. Appl Biochem Biotechnol 161(1):106–115.  https://doi.org/10.1007/s12010-009-8811-9 CrossRefPubMedGoogle Scholar
  114. Ullah A, Orij R, Brul S, Smits GJ (2012) Quantitative analysis of the modes of growth inhibition by weak organic acids in Saccharomyces cerevisiae. Appl Environ Microbiol 78(23):8377–8387.  https://doi.org/10.1128/AEM.02126-12 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Unrean P, Gätgens J, Klein B, Noack S, Champreda V (2018) Elucidating cellular mechanisms of Saccharomyces cerevisiae tolerant to combined lignocellulosic-derived inhibitors using high-throughput phenotyping and multiomics analyses. FEMS Yeast Res 18(8).  https://doi.org/10.1093/femsyr/foy106
  116. van den Hazel HB, Pichler H, do Valle Matta MA, Leitner E, Goffeau A, Daum G (1999) PDR16 and PDR17, two homologous genes of Saccharomyces cerevisiae, affect lipid biosynthesis and resistance to multiple drugs. J Biol Chem 274(4):1934–1941CrossRefGoogle Scholar
  117. Varga E, Klinke HB, Réczey K, Thomsen AB (2004) High solid simultaneous saccharification and fermentation of wet oxidized corn stover to ethanol. Biotechnol Bioeng 88:567–574.  https://doi.org/10.1002/bit.20222 CrossRefPubMedGoogle Scholar
  118. Verghese J, Abrams J, Wang Y, Morano KA (2012) Biology of the heat shock response and protein chaperones: budding yeast (Saccharomyces cerevisiae) as a model system. Microbiol Mol Biol Rev 76:115–158.  https://doi.org/10.1128/MMBR.05018-11 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Wallace-Salinas V, Signori L, Li Y-Y, Ask M, Bettiga M, Porro D, Thevelein JM, Branduardi P, Foulquié-Moreno MR, Gorwa-Grauslund M (2014) Re-assessment of YAP1 and MCR1 contributions to inhibitor tolerance in robust engineered Saccharomyces cerevisiae fermenting undetoxified lignocellulosic hydrolysate. AMB Express 4:56–56.  https://doi.org/10.1186/s13568-014-0056-5 CrossRefPubMedPubMedCentralGoogle Scholar
  120. Wang X, Liang Z, Hou J, Bao X, Shen Y (2016) Identification and functional evaluation of the reductases and dehydrogenases from Saccharomyces cerevisiae involved in vanillin resistance. BMC Biotechnol 16:31.  https://doi.org/10.1186/s12896-016-0264-y CrossRefPubMedPubMedCentralGoogle Scholar
  121. Wei S, Liu Y, Wu M, Ma T, Bai X, Hou J, Shen Y, Bao X (2018) Disruption of the transcription factors Thi2p and Nrm1p alleviates the post-glucose effect on xylose utilization in Saccharomyces cerevisiae. Biotechnol Biofuels 11:112.  https://doi.org/10.1186/s13068-018-1112-1 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Westman JO, Taherzadeh MJ, Franzén CJ (2012) Inhibitor tolerance and flocculation of a yeast strain suitable for second generation bioethanol production. Electron J Biotechnol 15(3).  https://doi.org/10.2225/vol15-issue3-fulltext-8
  123. Westman JO, Mapelli V, Taherzadeh MJ, Franzén CJ (2014) Flocculation causes inhibitor tolerance in Saccharomyces cerevisiae for second-generation bioethanol production. Appl Environ Microbiol 80:6908–6918.  https://doi.org/10.1128/AEM.01906-14 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Wimalasena TT, Greetham D, Marvin ME, Liti G, Chandelia Y, Hart A, Louis EJ, Phister TG, Tucker GA, Smart KA (2014) Phenotypic characterisation of Saccharomyces spp. yeast for tolerance to stresses encountered during fermentation of lignocellulosic residues to produce bioethanol. Microb Cell Factories 13:47.  https://doi.org/10.1186/1475-2859-13-47 CrossRefGoogle Scholar
  125. Woo JM, Yang KM, Kim SU, Blank LM, Park JB (2014) High temperature stimulates acetic acid accumulation and enhances the growth inhibition and ethanol production by Saccharomyces cerevisiae under fermenting conditions. Appl Microbiol Biotechnol 98:6085–6094.  https://doi.org/10.1007/s00253-014-5691-x CrossRefPubMedGoogle Scholar
  126. Wu G, Xu Z, Jonsson LJ (2017) Profiling of Saccharomyces cerevisiae transcription factors for engineering the resistance of yeast to lignocellulose-derived inhibitors in biomass conversion. Microb Cell Factories 16(1):199.  https://doi.org/10.1186/s12934-017-0811-9 CrossRefGoogle Scholar
  127. Xianxian Z, Juan T, Xu W, Ruoheng Y, Xiaoping Z, Yunfu G, Xi L, Menggen M (2015) YNL134C from Saccharomyces cerevisiae encodes a novel protein with aldehyde reductase activity for detoxification of furfural derived from lignocellulosic biomass. Yeast 32(5):409–422.  https://doi.org/10.1002/yea.3068 CrossRefGoogle Scholar
  128. Yáñez R, Romaní A, Garrote G, Alonso JL, Parajó JC (2009) Experimental evaluation of alkaline treatment as a method for enhancing the enzymatic digestibility of autohydrolysed Acacia dealbata. J Chem Technol Biotechnol 84(7):1070–1077.  https://doi.org/10.1002/jctb.2136 CrossRefGoogle Scholar
  129. Yu N, Tan L, Sun Z-Y, Tang Y-Q, Kida K (2018) Production of bio-ethanol by integrating microwave-assisted dilute sulfuric acid pretreated sugarcane bagasse slurry with molasses. Appl Biochem Biotechnol 185:191–206.  https://doi.org/10.1007/s12010-017-2651-9 CrossRefPubMedGoogle Scholar
  130. Zhang G-C, Liu J-J, Ding W-T (2012) Decreased xylitol formation during xylose fermentation in Saccharomyces cerevisiae due to overexpression of water-forming NADH oxidase. Appl Environ Microbiol 78(4):1081–1086.  https://doi.org/10.1128/aem.06635-11 CrossRefPubMedPubMedCentralGoogle Scholar
  131. Zhang G-C, Kong II, Wei N, Peng D, Turner TL, Sung BH, Sohn J, Jin Y (2016) Optimization of an acetate reduction pathway for producing cellulosic ethanol by engineered yeast. Biotechnol Bioeng 113:2587–2596.  https://doi.org/10.1002/bit.26021 CrossRefPubMedGoogle Scholar
  132. Zhou H, Zhu JY, Luo X, Leu S-Y, Wu X, Gleisner R, Dien BS, Hector RE, Yang D, Qiu X, Horn E, Negron J (2013) Bioconversion of beetle-killed lodgepole pine using sporl: process scale-up design, lignin coproduct, and high solids fermentation without detoxification. Ind Eng Chem Res 52:16057–16065.  https://doi.org/10.1021/ie402873y CrossRefGoogle Scholar
  133. Zhou Q, Liu ZL, Ning K, Wang A, Zeng X, Xu J (2014) Genomic and transcriptome analyses reveal that MAPK- and phosphatidylinositol-signaling pathways mediate tolerance to 5-hydroxymethyl-2-furaldehyde for industrial yeast Saccharomyces cerevisiae. Sci Rep 4:6556.  https://doi.org/10.1038/srep06556 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre of Biological Engineering (CEB)University of MinhoBragaPortugal
  2. 2.Institute for Bioengineering and Biosciences, Department of Bioengineering, Instituto Superior TécnicoUniversidade de LisboaLisbonPortugal

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