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Applied Microbiology and Biotechnology

, Volume 102, Issue 24, pp 10439–10456 | Cite as

Functions of aldehyde reductases from Saccharomyces cerevisiae in detoxification of aldehyde inhibitors and their biotechnological applications

  • Hanyu Wang
  • Qian Li
  • Xiaolin Kuang
  • Difan Xiao
  • Xuebing Han
  • Xiangdong Hu
  • Xi Li
  • Menggen Ma
Mini-Review
  • 199 Downloads

Abstract

Bioconversion of lignocellulosic biomass to high-value bioproducts by fermentative microorganisms has drawn extensive attentions worldwide. Lignocellulosic biomass cannot be efficiently utilized by microorganisms, such as Saccharomyces cerevisiae, but has to be pretreated prior to fermentation. Aldehyde compounds, as the by-products generated in the pretreatment process of lignocellulosic biomass, are considered as the most important toxic inhibitors to S. cerevisiae cells for their growth and fermentation. Aldehyde group in the aldehyde inhibitors, including furan aldehydes, aliphatic aldehydes, and phenolic aldehydes, is identified as the toxic factor. It has been demonstrated that S. cerevisiae has the ability to in situ detoxify aldehydes to their corresponding less or non-toxic alcohols. This reductive reaction is catalyzed by the NAD(P)H-dependent aldehyde reductases. In recent years, detoxification of aldehyde inhibitors by S. cerevisiae has been extensively studied and a huge progress has been made. This mini-review summarizes the classifications and structural features of the characterized aldehyde reductases from S. cerevisiae, their catalytic abilities to exogenous and endogenous aldehydes and effects of metal ions, chemical protective additives, and salts on enzyme activities, subcellular localization of the aldehyde reductases and their possible roles in protection of the subcellular organelles, and transcriptional regulation of the aldehyde reductase genes by the key stress-response transcription factors. Cofactor preference of the aldehyde reductases and their molecular mechanisms and efficient supply pathways of cofactors, as well as biotechnological applications of the aldehyde reductases in the detoxification of aldehyde inhibitors derived from pretreatment of lignocellulosic biomass, are also included or supplemented in this mini-review.

Keywords

Aldehyde reductase Classification Detoxification Inhibitor Localization Saccharomyces cerevisiae Transcriptional regulation 

Notes

Acknowledgments

The authors thank Prof. Dr. Alexander Steinbüchel, the Editor-in-Chief of Applied Microbiology and Biotechnology, for his kind invitation to write this mini-review.

Funding information

This work was funded by the National Natural Science Foundation of China (No. 31570086) and the Talent Introduction Fund of Sichuan Agricultural University (No. 01426100).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

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

References

  1. 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
  2. Almeida JRM, Röder A, Modig T, Laadan B, Lidén G, Gorwa-Grauslund MF (2008) NADH- vs NADPH-coupled reduction of 5-hydroxymethyl furfural (HMF) and its implications on product distribution in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 78(6):939–945.  https://doi.org/10.1007/s00253-008-1364-y CrossRefPubMedGoogle Scholar
  3. Alriksson B, Horváth IS, Jönsson LJ (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
  4. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402.  https://doi.org/10.1093/nar/25.17.3389 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bakker BM, Bro C, Kötter P, Luttik MAH, van Dijken JP, Pronk JT (2000) The mitochondrial alcohol dehydrogenase Adh3p is involved in a redox shuttle in Saccharomyces cerevisiae. J Bacteriol 182(17):4730–4737.  https://doi.org/10.1128/JB.182.17.4730-4737.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cavka A, Stagge S, Jönsson LJ (2015) Identification of small aliphatic aldehydes in pretreated lignocellulosic feedstocks and evaluation of their inhibitory effects on yeast. J Agric Food Chem 63(44):9747–9754.  https://doi.org/10.1021/acs.jafc.5b04803 CrossRefPubMedGoogle Scholar
  7. Chang Q, Griest TA, Harter TM, Petrash JM (2007) Functional studies of aldo-keto reductases in Saccharomyces cerevisiae. Biochim Biophys Acta 1773(3):321–329.  https://doi.org/10.1016/j.bbamcr.2006.10.009 CrossRefPubMedGoogle Scholar
  8. Chen CN, Porubleva L, Shearer G, Svrakic M, Holden LG, Dover JL, Johnston M, Chitnis PR, Kohl DH (2003) Associating protein activities with their genes: rapid identification of a gene encoding a methylglyoxal reductase in the yeast Saccharomyces cerevisiae. Yeast 20(6):545–554.  https://doi.org/10.1002/yea.979 CrossRefPubMedGoogle Scholar
  9. Drewke C, Ciriacy M (1988) Overexpression, purification and properties of alcohol dehydrogenase IV from Saccharomyces cerevisiae. Biochim Biophys Acta 950(1):54–60CrossRefGoogle Scholar
  10. Ford G, Ellis EM (2001) Three aldo-keto reductases of the yeast Saccharomyces cerevisiae. Chem Biol Interact 130–132(1–3):685–698.  https://doi.org/10.1016/S0009-2797(00)00259-3 CrossRefPubMedGoogle Scholar
  11. Ford G, Ellis EM (2002) Characterization of Ypr1p from Saccharomyces cerevisiae as a 2-methylbutyraldehyde reductase. Yeast 19(12):1087–1096.  https://doi.org/10.1002/yea.899 CrossRefPubMedGoogle Scholar
  12. Garreau H, Hasan RN, Renault G, Estruch F, Boy-Marcotte E, Jacquet M (2000) Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology 146(Pt 9):2113–2120.  https://doi.org/10.1099/00221287-146-9-2113 CrossRefPubMedGoogle Scholar
  13. 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
  14. Grey M, Schmidt M, Brendel M (1996) Overexpression of ADH1 confers hyper-resistance to formaldehyde in Saccharomyces cerevisiae. Curr Genet 29(5):437–440.  https://doi.org/10.1007/s002940050068 CrossRefPubMedGoogle Scholar
  15. Gulshan K, Rovinsky SA, Coleman ST, Moye-Rowley WS (2005) Oxidant-specific folding of Yap1p regulates both transcriptional activation and nuclear localization. J Biol Chem 280(49):40524–40533.  https://doi.org/10.1074/jbc.M504716200 CrossRefPubMedGoogle Scholar
  16. Guo PC, Bao ZZ, Ma XX, Xia Q, Li WF (2014) Structural insights into the cofactor-assisted substrate recognition of yeast methylglyoxal/isovaleraldehyde reductase Gre2. Biochim Biophys Acta 1844(9):1486–1492.  https://doi.org/10.1016/j.bbapap.2014.05.008 CrossRefPubMedGoogle Scholar
  17. Gutiérrez T, Buszko ML, Ingram LO, Preston JF (2002) Reduction of furfural to furfuryl alcohol by ethanologenic strains of bacteria and its effect on ethanol production from xylose. Appl Biochem Biotechnol 98–100:327–340.  https://doi.org/10.1385/ABAB:98-100:1-9:327 CrossRefPubMedGoogle Scholar
  18. Hashikawa N, Mizukami Y, Imazu H, Sakurai H (2006) Mutated yeast heat shock transcription factor activates transcription independently of hyperphosphorylation. J Biol Chem 281(7):3936–3942.  https://doi.org/10.1074/jbc.M510827200 CrossRefPubMedGoogle Scholar
  19. Hauser M, Horn P, Tournu H, Hauser NC, Hoheisel JD, Brown AJ, Dickinson JR (2007) A transcriptome analysis of isoamyl alcohol-induced filamentation in yeast reveals a novel role for Gre2p as isovaleraldehyde reductase. FEMS Yeast Res 7(1):84–92.  https://doi.org/10.1111/j.1567-1364.2006.00151.x CrossRefPubMedGoogle Scholar
  20. Hazelwood LA, Daran JM, van Maris AJ, Pronk JT, Dickinson JR (2008) The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74(8):2259–2266.  https://doi.org/10.1128/AEM.02625-07 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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
  22. Hossain MZ, Teixeira da Silva JA, Fujita M (2006) Differential roles of glutathione S-transferase in oxidative stress modulation. In: Teixeira da Silva JA (ed) Floriculture, Ornamental and Plant Biotechnology. Advances and Topical Issues. Global Science Books Ltd, London, pp 108–116Google Scholar
  23. Hu J, Lin Y, Zhang Z, Xiang T, Mei Y, Zhao S, Liang Y, Peng N (2016) High-titer lactic acid production by Lactobacillus pentosus FL0421 from corn stover using fed-batch simultaneous saccharification and fermentation. Bioresour Technol 214:74–80.  https://doi.org/10.1016/j.biortech.2016.04.034 CrossRefPubMedGoogle Scholar
  24. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK (2003) Global analysis of protein localization in budding yeast. Nature 425(6959):686–691.  https://doi.org/10.1038/nature02026 CrossRefPubMedGoogle Scholar
  25. Jayakody LN, Hayashi N, Kitagaki H (2011) Identification of glycolaldehyde as the key inhibitor of bioethanol fermentation by yeast and genome-wide analysis of its toxicity. Biotechnol Lett 33(2):285–292.  https://doi.org/10.1007/s10529-010-0437-z CrossRefPubMedGoogle Scholar
  26. Jayakody LN, Horie K, Hayashi N, Kitagaki H (2013) Engineering redox cofactor utilization for detoxification of glycolaldehyde, a key inhibitor of bioethanol production, in yeast Saccharomyces cerevisiae. Appl Microbiol Biotechnol 97(14):6589–6600.  https://doi.org/10.1007/s00253-013-4997-4 CrossRefPubMedGoogle Scholar
  27. Jez JM, Penning TM (2001) The aldo-keto reductase (AKR) superfamily: an update. Chem Biol Interact 130–132(1–3):499–525.  https://doi.org/10.1016/S0009-2797(00)00295-7 CrossRefPubMedGoogle Scholar
  28. Joe MH, Kim JY, Lim S, Kim DH, Bai S, Park H, Lee SG, Han SJ, Choi JI (2015) Microalgal lipid production using the hydrolysates of rice straw pretreated with gamma irradiation and alkali solution. Biotechnol Biofuels 8:125.  https://doi.org/10.1186/s13068-015-0308-x CrossRefPubMedPubMedCentralGoogle Scholar
  29. Jönsson LJ, Alriksson B, Nilvebrant NO (2013) Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels 6(1):16.  https://doi.org/10.1186/1754-6834-6-16 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kavanagh KL, Jornvall H, Persson B, Oppermann U (2008) Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell Mol Life Sci 65(24):3895–3906.  https://doi.org/10.1007/s00018-008-8588-y CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kuhn A, van Zyl C, van Tonder A, Prior BA (1995) Purification and partial characterization of an aldo-keto reductase from Saccharomyces cerevisiae. Appl Environ Microbiol 61(4):1580–1585PubMedPubMedCentralGoogle Scholar
  32. Laadan B, Almeida JR, Rådström P, Hahn-Hägerdal B, Gorwa-Grauslund M (2008) Identification of an NADH-dependent 5-hydroxymethylfurfural-reducing alcohol dehydrogenase in Saccharomyces cerevisiae. Yeast 25(3):191–198.  https://doi.org/10.1002/yea.1578 CrossRefPubMedGoogle Scholar
  33. Larroy C, Fernández M, González E, Parés X, Biosca JA (2002a) Characterization of the Saccharomyces cerevisiae YMR318C (ADH6) gene product as a broad specificity NADPH-dependent alcohol dehydrogenase: relevance in aldehyde reduction. Biochem J 361(Pt 1):163–172.  https://doi.org/10.1042/0264-6021:3610163 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Larroy C, Parés X, Biosca JA (2002b) Characterization of a Saccharomyces cerevisiae NADP(H)-dependent alcohol dehydrogenase (ADHVII), a member of the cinnamyl alcohol dehydrogenase family. Eur J Biochem 269(22):5738–5745.  https://doi.org/10.1046/j.1432-1033.2002.03296.x CrossRefPubMedGoogle Scholar
  35. Leskovac V, Trivić S, Peričin D (2002) The three zinc-containing alcohol dehydrogenases from baker’s yeast, Saccharomyces cerevisiae. FEMS Yeast Res 2(4):481–494.  https://doi.org/10.1111/j.1567-1364.2002.tb00116.x CrossRefPubMedGoogle Scholar
  36. Li X, Yang R, Ma M, Wang X, Tang J, Zhao X, Zhang X (2015) A novel aldehyde reductase encoded by YML131W from Saccharomyces cerevisiae confers tolerance to furfural derived from lignocellulosic biomass conversion. Bioenerg Res 8(1):119–129.  https://doi.org/10.1007/s12155-014-9506-9 CrossRefGoogle Scholar
  37. Liu ZL (2011) Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl Microbiol Biotechnol 90(3):809–825.  https://doi.org/10.1007/s00253-011-3167-9 CrossRefPubMedGoogle Scholar
  38. Liu ZL (2018) Understanding the tolerance of the industrial yeast Saccharomyces cerevisiae against a major class of toxic aldehyde compounds. Appl Microbiol Biotechnol 102(13):5369–5390.  https://doi.org/10.1007/s00253-018-8993-6 CrossRefPubMedGoogle Scholar
  39. 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
  40. 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
  41. 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
  42. Liu ZL, Ma M, Song M (2009) Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Mol Gen Genomics 282(3):233–244.  https://doi.org/10.1007/s00438-009-0461-7 CrossRefGoogle Scholar
  43. van Loon AP, Young ET (1986) Intracellular sorting of alcohol dehydrogenase isoenzymes in yeast: a cytosolic location reflects absence of an amino-terminal targeting sequence for the mitochondrion. EMBO J 5(1):161–165CrossRefGoogle Scholar
  44. 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.  https://doi.org/10.1186/1471-2164-11-660 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Marbaix AY, Noël G, Detroux AM, Vertommen D, Van Schaftingen E, Linster CL (2011) Extremely conserved ATP- or ADP-dependent enzymatic system for nicotinamide nucleotide repair. J Biol Chem 286(48):41246–41252.  https://doi.org/10.1074/jbc.C111.310847 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, Feldblyum TV, White O, Paulsen IT, Nierman WC, Lee J, Szczypinski B, Fraser CM (2003) Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4-related bacteriophage. J Bacteriol 185(17):5220–5233.  https://doi.org/10.1128/JB.185.17.5220-5233.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Moon J, Liu ZL (2012) Engineered NADH-dependent GRE2 from Saccharomyces cerevisiae by directed enzyme evolution enhances HMF reduction using additional cofactor NADPH. Enzym Microb Technol 50(2):115–120.  https://doi.org/10.1016/j.enzmictec.2011.10.007 CrossRefGoogle Scholar
  48. Moon J, Liu ZL (2015) Direct enzyme assay evidence confirms aldehyde reductase function of Ydr541cp and Ygl039wp from Saccharomyces cerevisiae. Yeast 32(4):399–407.  https://doi.org/10.1002/yea.3067 CrossRefPubMedGoogle Scholar
  49. Nguyen TTM, Iwaki A, Izawa S (2015) The ADH7 promoter of Saccharomyces cerevisiae is vanillin-inducible and enables mRNA translation under severe vanillin stress. Front Microbiol 6:1390.  https://doi.org/10.3389/fmicb.2015.01390 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nordling E, Jörnvall H, Persson B (2002) Medium-chain dehydrogenases/reductases (MDR). Family characterizations including genome comparisons and active site modeling. Eur J Biochem 269(17):4267–4276.  https://doi.org/10.1046/j.1432-1033.2002.03114.x CrossRefPubMedGoogle Scholar
  51. Oppermann UC, Maser E (2000) Molecular and structural aspects of xenobiotic carbonyl metabolizing enzymes. Role of reductases and dehydrogenases in xenobiotic phase I reactions. Toxicology 144(1–3):71–81.  https://doi.org/10.1016/S0300-483X(99)00192-4 CrossRefPubMedGoogle Scholar
  52. Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74(1):25–33.  https://doi.org/10.1016/S0960-8524(99)00161-3 CrossRefGoogle Scholar
  53. Parawira W, Tekere M (2011) Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 31(1):20–31.  https://doi.org/10.3109/07388551003757816 CrossRefPubMedGoogle Scholar
  54. Park SE, Koo HM, Park YK, Park SM, Park JC, Lee OK, Park YC, Seo JH (2011) Expression of aldehyde dehydrogenase 6 reduces inhibitory effect of furan derivatives on cell growth and ethanol production in Saccharomyces cerevisiae. Bioresour Technol 102(10):6033–6038.  https://doi.org/10.1016/j.biortech.2011.02.101 CrossRefPubMedGoogle Scholar
  55. Persson B, Jeffery J, Jörnvall H (1991) Different segment similarities in long-chain dehydrogenases. Biochem Biophys Res Commun 177(1):218–223.  https://doi.org/10.1016/0006-291X(91)91970-N CrossRefPubMedGoogle Scholar
  56. Persson B, Hedlund J, Jörnvall H (2008) Medium- and short-chain dehydrogenase/reductase gene and protein families: the MDR superfamily. Cell Mol Life Sci 65(24):3879–3894.  https://doi.org/10.1007/s00018-008-8587-z CrossRefPubMedPubMedCentralGoogle Scholar
  57. Persson B, Kallberg Y, Bray JE, Bruford E, Dellaporta SL, Favia AD, Duarte RG, Jörnvall H, Kavanagh KL, Kedishvili N, Kisiela M, Maser E, Mindnich R, Orchard S, Penning TM, Thornton JM, Adamski J, Oppermann U (2009) The SDR (short-chain dehydrogenase/reductase and related enzymes) nomenclature initiative. Chem Biol Interact 178(1–3):94–98.  https://doi.org/10.1016/j.cbi.2008.10.040 CrossRefPubMedGoogle Scholar
  58. Petersson A, Almeida JR, Modig T, Karhumaa K, Hahn- Hägerdal B, Gorwa-Grauslund MF, Lidén G (2006) A 5-hydroxymethyl furfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23(6):455–464.  https://doi.org/10.1002/yea.1370 CrossRefPubMedGoogle Scholar
  59. Petrash JM, Murthy BS, Young M, Morris K, Rikimaru L, Griest TA, Harter T (2001) Functional genomic studies of aldo-keto reductases. Chem Biol Interact 130–132(1–3):673–683.  https://doi.org/10.1016/S0009-2797(00)00258-1 CrossRefPubMedGoogle Scholar
  60. Rabemanolontsoa H, Saka S (2016) Various pretreatments of lignocellulosics. Bioresour Technol 199:83–91.  https://doi.org/10.1016/j.biortech.2015.08.029 CrossRefPubMedGoogle Scholar
  61. Raj SB, Ramaswamy S, Plapp BV (2014) Yeast alcohol dehydrogenase structure and catalysis. Biochemistry 53(36):5791–5803.  https://doi.org/10.1021/bi5006442 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Reifenrath M, Boles E (2018) Engineering of hydroxymandelate synthases and the aromatic amino acid pathway enables de novo biosynthesis of mandelic and 4-hydroxymandelic acid with Saccharomyces cerevisiae. Metab Eng 45:246–254.  https://doi.org/10.1016/j.ymben.2018.01.001 CrossRefPubMedGoogle Scholar
  63. Revollo JR, Grimm AA, Imai S (2004) The NAD biosynthesis pathway mediated by nicotinamide phosphoribosyltransferase regulates Sir2 activity in mammalian cells. J Biol Chem 279(49):50754–50763.  https://doi.org/10.1074/jbc.M408388200 CrossRefPubMedGoogle Scholar
  64. Riveros-Rosas H, Julián-Sánchez A, Villalobos-Molina R, Pardo JP, Piña E (2003) Diversity, taxonomy and evolution of medium-chain dehydrogenase/reductase superfamily. Eur J Biochem 270(16):3309–3334.  https://doi.org/10.1046/j.1432-1033.2003.03704.x CrossRefPubMedGoogle Scholar
  65. Rongvaux A, Andris F, Van Gool F, Leo O (2003) Reconstructing eukaryotic NAD metabolism. Bioessays 25(7):683–690.  https://doi.org/10.1002/bies.10297 CrossRefPubMedGoogle Scholar
  66. Sasano Y, Watanabe D, Ukibe K, Inai T, Ohtsu I, Shimoi H, Takagi H (2012) Overexpression of the yeast transcription activator Msn2 confers furfural resistance and increases the initial fermentation rate in ethanol production. J Biosci Bioeng 113(4):451–455.  https://doi.org/10.1016/j.jbiosc.2011.11.017 CrossRefPubMedGoogle Scholar
  67. Sehnem NT, Machado Ada S, Leite FC, Pita Wde B, de Morais MA Jr, Ayub MA (2013) 5-Hydroxymethylfurfural induces ADH7 and ARI1 expression in tolerant industrial Saccharomyces cerevisiae strain P6H9 during bioethanol production. Bioresour Technol 133:190–196.  https://doi.org/10.1016/j.biortech.2013.01.063 CrossRefPubMedGoogle Scholar
  68. Shen Y, Li H, Wang X, Zhang X, Hou J, Wang L, Gao N, Bao X (2014) High vanillin tolerance of an evolved Saccharomyces cerevisiae strain owing to its enhanced vanillin reduction and antioxidative capacity. J Ind Microbiol Biotechnol 41(11):1637–1645.  https://doi.org/10.1007/s10295-014-1515-3 CrossRefPubMedGoogle Scholar
  69. Smith MG, Des Etages SG, Snyder M (2004) Microbial synergy via an ethanol-triggered pathway. Mol Cell Biol 24(9):3874–3884.  https://doi.org/10.1128/MCB.24.9.3874-3884.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Valencia E, Larroy C, Ochoa WF, Parés X, Fita I, Biosca JA (2004) Apo and Holo structures of an NADPH-dependent cinnamyl alcohol dehydrogenase from Saccharomyces cerevisiae. J Mol Biol 341(4):1049–1062.  https://doi.org/10.1016/j.jmb.2004.06.037 CrossRefPubMedGoogle Scholar
  71. Vasiliou V, Pappa A, Petersen D (2000) Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem Biol Interact 129:1–2):1–19.  https://doi.org/10.1016/S0009-2797(00)00211-8 CrossRefPubMedGoogle Scholar
  72. Voulgaridou GP, Anestopoulos I, Franco R, Panayiotidis MI, Pappa A (2011) DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res 711(1–2):13–27.  https://doi.org/10.1016/j.mrfmmm.2011.03.006 CrossRefPubMedGoogle Scholar
  73. Wahlbom CF, Hahn-Hägerdal B (2002) Furfural, 5-hydroxymethyl furfural, and acetoin act as external electron acceptors during anaerobic fermentation of xylose in recombinant Saccharomyces cerevisiae. Biotechnol Bioeng 78(2):172–178.  https://doi.org/10.1002/bit.10188.abs CrossRefPubMedGoogle Scholar
  74. Walton JD, Paquin CE, Kaneko K, Williamson VM (1986) Resistance to antimycin A in yeast by amplification of ADH4 on a linear, 42 kb palindromic plasmid. Cell 46(6):857–863.  https://doi.org/10.1016/0092-8674(86)90067-X CrossRefPubMedGoogle Scholar
  75. Wang X, Li BZ, Ding MZ, Zhang WW, Yuan YJ (2013) Metabolomic analysis reveals key metabolites related to the rapid adaptation of Saccharomyces cerevisiae to multiple inhibitors of furfural, acetic acid, and phenol. OMICS 17(3):150–159.  https://doi.org/10.1089/omi.2012.0093 CrossRefPubMedGoogle Scholar
  76. 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
  77. Wang HY, Xiao DF, Zhou C, Wang LL, Wu L, Lu YT, Xiang QJ, Zhao K, Li X, Ma MG (2017a) YLL056C from Saccharomyces cerevisiae encodes a novel protein with aldehyde reductase activity. Appl Microbiol Biotechnol 101(11):4507–4520.  https://doi.org/10.1007/s00253-017-8209-5 CrossRefPubMedGoogle Scholar
  78. Wang H, Ouyang Y, Zhou C, Xiao D, Guo Y, Wu L, Li X, Gu Y, Xiang Q, Zhao K, Yu X, Zou L, Ma M (2017b) YKL071W from Saccharomyces cerevisiae encodes a novel aldehyde reductase for detoxification of glycolaldehyde and furfural derived from lignocellulose. Appl Microbiol Biotechnol 101(23–24):8405–8418.  https://doi.org/10.1007/s00253-017-8567-z CrossRefPubMedGoogle Scholar
  79. Wu G, Xu Z, Jönsson 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
  80. Yang DD, de Billerbeck GM, Zhang JJ, Rosenzweig F, Francois JM (2018) Deciphering the origin, evolution, and physiological function of the subtelomeric aryl-alcohol dehydrogenase gene family in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 84(1):e01553–e01517.  https://doi.org/10.1128/AEM.01553-17 CrossRefPubMedGoogle Scholar
  81. Yasokawa D, Murata S, Iwahashi Y, Kitagawa E, Nakagawa R, Hashido T, Iwahashi H (2010) Toxicity of methanol and formaldehyde towards Saccharomyces cerevisiae as assessed by DNA microarray analysis. Appl Biochem Biotechnol 160(6):1685–1698.  https://doi.org/10.1007/s12010-009-8684-y CrossRefPubMedGoogle Scholar
  82. Yi X, Gu H, Gao Q, Liu ZL, Bao J (2015) Transcriptome analysis of Zymomonas mobilis ZM4 reveals mechanisms of tolerance and detoxification of phenolic aldehyde inhibitors from lignocellulose pretreatment. Biotechnol Biofuels 8:153.  https://doi.org/10.1186/s13068-015-0333-9 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Yofe I, Weill U, Meurer M, Chuartzman S, Zalckvar E, Goldman O, Ben-Dor S, Schütze C, Wiedemann N, Knop M, Khmelinskii A, Schuldiner M (2016) One library to make them all: streamlining the creation of yeast libraries via a SWAp-tag strategy. Nat Methods 13(4):371–378.  https://doi.org/10.1038/nmeth.3795 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Zahed O, Jouzani GS, Abbasalizadeh S, Khodaiyan F, Tabatabaei M (2016) Continuous co-production of ethanol and xylitol from rice straw hydrolysate in a membrane bioreactor. Folia Microbiol (Praha) 61(3):179–189.  https://doi.org/10.1007/s12223-015-0420-0 CrossRefGoogle Scholar
  85. Zhao X, Tang J, Wang X, Yang R, Zhang X, Gu Y, Li X, Ma 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 CrossRefPubMedGoogle Scholar
  86. Zhu J, Rong Y, Yang J, Zhou X, Xu Y, Zhang L, Chen J, Yong Q, Yu S (2015) Integrated production of xylonic acid and bioethanol from acid-catalyzed steam-exploded corn stover. Appl Biochem Biotechnol 176(5):1370–1381.  https://doi.org/10.1007/s12010-015-1651-x CrossRefPubMedGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Hanyu Wang
    • 1
  • Qian Li
    • 1
  • Xiaolin Kuang
    • 1
  • Difan Xiao
    • 1
  • Xuebing Han
    • 1
  • Xiangdong Hu
    • 1
  • Xi Li
    • 2
  • Menggen Ma
    • 1
    • 3
  1. 1.Institute of Natural Resources and Geographic Information Technology, College of ResourcesSichuan Agricultural UniversityChengduPeople’s Republic of China
  2. 2.College of Landscape ArchitectureSichuan Agricultural UniversityChengduPeople’s Republic of China
  3. 3.Department of Applied Microbiology, College of ResourcesSichuan Agricultural UniversityChengduPeople’s Republic of China

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