Re-assessment of YAP1 and MCR1 contributions to inhibitor tolerance in robust engineered Saccharomyces cerevisiae fermenting undetoxified lignocellulosic hydrolysate

AMB Express

Volumn 4, Issue 1, 2014, Pages 1-12

  Wallace Salinas, Valeria ^a   Signori, Lorenzo ^b   Li, Ying Ying ^c,d   Ask, Magnus ^e   Bettiga, Maurizio ^e   Porro, Danilo ^b   Thevelein, Johan M ^c,d   Branduardi, Paola ^b   Foulquié Moreno, María R ^c,d   Gorwa Grauslund, Marie ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Ethanol; Hydrolysate; Inhibitors; MCR1; Saccharomyces cerevisiae; YAP1

Indexed keywords

CYTOCHROME B5 REDUCTASE; FURFURAL; LIGNOCELLULOSIC HYDROLYSATE; STARCH HYDROLYSATE; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG; XYLOSE;

ARTICLE; BIOMASS PRODUCTION; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DNA MODIFICATION; ELECTROPORATION; FERMENTATION; FUNGAL STRAIN; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC ENGINEERING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOLECULAR BIOLOGY; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE;

EID: 84947046745     PISSN: None     EISSN: 21910855     Source Type: Journal    
DOI: 10.1186/s13568-014-0056-5     Document Type: Article

References (50)

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. Biotechnology for Biofuels 3:2. doi:10.1186/1754-6834-3-2
2. Almeida JRM, Bertilsson M, Gorwa-Grauslund MF, Gorsich S, Lidén G (2009a) Metabolic effects of furaldehydes and impacts on biotechnological processes. Appl Microbiol Biotechnol 82(4):625–638. doi:10.1007/s00253-009-1875-1
3. Almeida JRM, Karhumaa K, Bengtsson O, Gorwa-Grauslund M-F (2009b) Screening of Saccharomyces cerevisiae strains with respect to anaerobic growth in non-detoxified lignocellulose hydrolysate. Bioresour Technol 100(14):3674–3677. doi:http://dx.doi.org/10.1016/j.biortech.2009.02.057
4. Almeida JRM, Runquist D, Sànchez Nogué V, Lidén G, Gorwa-Grauslund MF (2011) Stress-related challenges in pentose fermentation to ethanol by the yeast Saccharomyces cerevisiae. Biotechnol J 6(3):286–299. doi:10.1002/biot.201000301
5. 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. doi:10.1016/j.procbio.2009.09.016
6. Ask M, Bettiga M, Duraiswamy V, Olsson L (2013) Pulsed addition of HMF and furfural to batch-grown xylose-utilizing Saccharomyces cerevisiae results in different physiological responses in glucose and xylose consumption phase. Biotechnology for Biofuels 6(1):181
7. Bellissimi E, van Dijken JP, Pronk JT, van Maris AJA (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. doi:10.1111/j.1567-1364.2009.00487.x
8. Benatuil L, Perez JM, Belk J, Hsieh CM (2010) An improved yeast transformation method for the generation of very large human antibody libraries. Protein Eng Des Sel 23(4):155–159. doi:10.1093/protein/gzq002
9. Bengtsson O, Hahn-Hagerdal B, Gorwa-Grauslund M (2009) Xylose reductase from Pichia stipitis with altered coenzyme preference improves ethanolic xylose fermentation by recombinant Saccharomyces cerevisiae. Biotechnology for Biofuels 2(1):9
10. Bergdahl B, Heer D, Sauer U, Hahn-Hägerdal B, van Niel EW (2012) Dynamic metabolomics differentiates between carbon and energy starvation in recombinant Saccharomyces cerevisiae fermenting xylose. Biotechnology for Biofuels 5(1):34
11. Branduardi P, Fossati T, Sauer M, Pagani R, Mattanovich D, Porro D (2007) Biosynthesis of vitamin C by yeast leads to increased stress resistance. PLoS One 2(10):e1092. doi:10.1371/journal.pone.0001092
12. Brat D, Boles E, Wiedemann B (2009) Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl Environ Microbiol 75(8):2304–2311. doi:AEM.02522-08
13. Casey E, Sedlak M, Ho NWY, Mosier NS (2010) Effect of acetic acid and pH on the cofermentation of glucose and xylose to ethanol by a genetically engineered strain of Saccharomyces cerevisiae. FEMS Yeast Res 10(4):385–393. doi:10.1111/j.1567-1364.2010.00623.x
14. Demeke MM, Dietz H, Li Y, Foulquie-Moreno MR, Mutturi S, Deprez S, Den Abt T, Bonini BM, Lidén 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. Biotechnology for Biofuels 6(1):89. doi:10.1186/1754-6834-6-89
15. Demeke MM, Dumortier F, Li Y, Broeckx T, Foulquie-Moreno MR, Thevelein JM (2013b) Combining inhibitor tolerance and D-xylose fermentation in industrial Saccharomyces cerevisiae for efficient lignocellulose-based bioethanol production. Biotechnology for Biofuels 6(1):120. doi:10.1186/1754-6834-6-120
16. DeRisi JL, Iyer VR, Brown PO (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278(5338):680–686
17. Feng X, Zhao H (2013) Investigating xylose metabolism in recombinant Saccharomyces cerevisiae via 13C metabolic flux analysis. Microb Cell Fact 12(1):114
18. Gietz RD, Schiestl RH, Willems AR, Woods RA (1995) Studies on the transformation of intact yeast cells by the LiAc/s-DNA/PEG procedure. Yeast 11(4):355–360
19. Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30(6):e23. doi:10.1093/nar/30.6.e23
20. Güldener U, Heck S, Fiedler T, Beinhauer J, Hegemann JH (1996) A New efficient gene disruption cassette for repeated Use in budding yeast. Nucleic Acids Res 24(13):2519–2524. doi:10.1093/nar/24.13.2519
21. Hahne K, Haucke V, Ramage L, Schatz G (1994) Incomplete arrest in the outer membrane sorts NADH-cytochrome b5 reductase to two different submitochondrial compartments. Cell 79(5):829–839. doi:http://dx.doi.org/10.1016/0092-8674(94)90072-8
22. Haitani Y, Tanaka K, Yamamoto M, Nakamura T, Ando A, Ogawa J, Shima J (2012) Identification of an acetate-tolerant strain of Saccharomyces cerevisiae and characterization by gene expression analysis. J Biosci Bioeng 114(6):648–651. doi:10.1016/j.jbiosc.2012.07.002
23. Helle S, Cameron D, Lam J, White B, Duff S (2003) Effect of inhibitory compounds found in biomass hydrolysates on growth and xylose fermentation by a genetically engineered strain of S. cerevisiae. Enzyme Microb Technol 33(6):786–792. doi:10.1016/S0141-0229(03)00214-X
24. Herrero E, Ros J, Belli G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780(11):1217–1235. doi:10.1016/j.bbagen.2007.12.004
25. Hill J, Donald KA, Griffiths DE (1991) DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res 19(20):5791
26. Jeppsson M, Johansson B, Jensen PR, Hahn-Hägerdal B, Gorwa-Grauslund MF (2003) The level of glucose-6-phosphate dehydrogenase activity strongly influences xylose fermentation and inhibitor sensitivity in recombinant Saccharomyces cerevisiae strains. Yeast 20(15):1263–1272. doi:10.1002/yea.1043
27. Jun H, Kieselbach T, Jonsson L (2012) Comparative proteome analysis of Saccharomyces cerevisiae: a global overview of in vivo targets of the yeast activator protein 1. BMC Genomics 13(1):230
28. Kim D, Hahn J-S (2013) Roles of Yap1 transcription factor and antioxidants in yeast tolerance to furfural and 5-hydroxymetylfurfural that function as thiol-reactive electrophiles generating oxidative stress. Appl Environ Microbiol 79(16):5069–5077. doi:10.1128/aem.00643-13
29. Lee J-S, Huh W-K, Lee B-H, Baek Y-U, Hwang C-S, Kim S-T, Kim Y-R, Kang S-O (2001) Mitochondrial NADH-cytochrome b5 reductase plays a crucial role in the reduction of d-erythroascorbyl free radical in Saccharomyces cerevisiae. Biochim Biophys Acta Gen Subj 1527(1–2):31–38. doi:http://dx.doi.org/10.1016/S0304-4165(01)00134-9
30. Liu Z (2011) Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl Microbiol Biotechnol 90(3):809–825. doi:10.1007/s00253-011-3167-9
31. Liu ZL, Slininger P, Gorsich S (2005) Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 121(1–3):451–460. doi:10.1385/abab:121:1-3:0451
32. 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(1):660
33. Martin C, Jönsson LJ (2003) Comparison of the resistance of industrial and laboratory strains of Saccharomyces and Zygosaccharomyces to lignocellulose-derived fermentation inhibitors. Enzyme Microb Technol 32(3–4):386–395. doi:http://dx.doi.org/10.1016/S0141-0229(02)00310-1
34. Matsushika A, Nagashima A, Goshima T, Hoshino T (2013) Fermentation of xylose causes inefficient metabolic state Due to carbon/energy starvation and reduced glycolytic flux in recombinant industrial Saccharomyces cerevisiae. PLoS One 8(7):e69005. doi:10.1371/journal.pone.0069005
35. Meineke B, Engl G, Kemper C, Vasiljev-Neumeyer A, Paulitschke H, Rapaport D (2008) The outer membrane form of the mitochondrial protein Mcr1 follows a TOM-independent membrane insertion pathway. FEBS Lett 582(6):855–860. doi:http://dx.doi.org/10.1016/j.febslet.2008.02.009
36. Mira N, Palma M, Guerreiro J, Sa-Correia I (2010) Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid. Microb Cell Fact 9(1):79
37. Mumberg D, Muller R, Funk M (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156(1):119–122
38. Nguyen TTM, Iwaki A, Ohya Y, Izawa S (2014) Vanillin causes the activation of Yap1 and mitochondrial fragmentation in Saccharomyces cerevisiae. J Biosci Bioeng 117(1):33–38. doi:http://dx.doi.org/10.1016/j.jbiosc.2013.06.008
39. Parawira W, Tekere M (2011) Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 31(1):20–31. doi:10.3109/07388551003757816
40. Petersson A, Almeida JRM, 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. doi:10.1002/yea.1370
41. Sambrook J, Russel D (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA
42. Semchyshyn HM, Abrat OB, Miedzobrodzki J, Inoue Y, Lushchak V (2011) Acetate but not propionate induces oxidative stress in bakers’ yeast Saccharomyces cerevisiae. Redox Rep 16(1):15–23
43. Subtil T, Boles E (2012) Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnology for Biofuels 5(1):14
44. Sundström L, Larsson S, Jönsson L (2010) Identification of Saccharomyces cerevisiae genes involved in the resistance to Phenolic fermentation inhibitors. Appl Biochem Biotechnol 161(1–8):106–115. doi:10.1007/s12010-009-8811-9
45. Swinnen S, Schaerlaekens K, Pais T, Claesen J, Hubmann G, Yang Y, Demeke M, Foulquié-Moreno MR, Goovaerts A, Souvereyns K, Clement L, Dumortier F, Thevelein JM (2012) Identification of novel causative genes determining the complex trait of high ethanol tolerance in yeast using pooled-segregant whole-genome sequence analysis. Genome Res 22(5):975–984. doi:10.1101/gr.131698.111
46. Toone WM, Jones N (1999) AP-1 transcription factors in yeast. Curr Opin Genet Dev 9(1):55–61. doi:http://dx.doi.org/10.1016/S0959-437X(99)80008-2
47. van Dijken JP, Bauer J, Brambilla L, Duboc P, Francois JM, Gancedo C, Giuseppin MLF, Heijnen JJ, Hoare M, Lange HC, Madden EA, Niederberger P, Nielsen J, Parrou JL, Petit T, Porro D, Reuss M, van Riel N, Rizzi M, Steensma HY, Verrips CT, Vindeløv J, Pronk JT (2000) An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains. Enzyme Microb Technol 26(9–10):706–714. doi:http://dx.doi.org/10.1016/S0141-0229(00)00162-9
48. Verduyn C, Postma E, Scheffers WA, van Dijken JP (1992) Effect of benzoic acid on metabolic fluxes in yeasts - a continuous culture study on the regulation of respiration and alcoholic fermentation. Yeast 8(7):501–517
49. Wahlbom CF, Eliasson A, Hahn-Hägerdal B (2001) Intracellular fluxes in a recombinant xylose-utilizing Saccharomyces cerevisiae cultivated anaerobically at different dilution rates and feed concentrations. Biotechnol Bioeng 72(3):289–296. doi:10.1002/1097-0290(20010205)72:3<289::aid-bit5>3.0.co;2-9
50. Wang X, Jin M, Balan V, Jones AD, Li X, Li B-Z, Dale BE, Yuan Y-J (2014) Comparative metabolic profiling revealed limitations in xylose-fermenting yeast during co-fermentation of glucose and xylose in the presence of inhibitors. Biotechnol Bioeng 111(1):152–164. doi:10.1002/bit.24992