Improved xylose metabolism by a CYC8 mutant of Saccharomyces cerevisiae

Applied and Environmental Microbiology

Volumn 83, Issue 11, 2017, Pages

  Nijland, Jeroen G ^a   Shin, Hyun Yong ^a   Boender, Leonie G M ^b   De Waal, Paul P ^b   Klaassen, Paul ^b   Driessen, Arnold J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b DSM BIOTECHNOLOGY CENTER   (Netherlands)

Author keywords

Evolutionary engineering; Sugar transporter; Transcriptome; Xylose transport; Yeast

Indexed keywords

CELLS; CYTOLOGY; GENE EXPRESSION; GENES; GLUCOSE; METABOLISM; PHYSIOLOGY; WALL FUNCTION; YEAST;

EVOLUTIONARY ENGINEERING; HEXOSE TRANSPORTERS; MULTIGENE FAMILIES; SECOND GENERATION BIOETHANOL; SUGAR TRANSPORTERS; TRANSCRIPTOME ANALYSIS; TRANSCRIPTOMES; XYLOSE TRANSPORT;

XYLOSE;

CONCENTRATION (COMPOSITION); GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ENGINEERING; GENOME; GENOMICS; METABOLISM; MUTATION; SUGAR; YEAST;

SACCHAROMYCES CEREVISIAE;

CYC8 PROTEIN, S CEREVISIAE; GLUCOSE; GLUCOSE TRANSPORTER; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; XYLOSE;

FERMENTATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MISSENSE MUTATION; SACCHAROMYCES CEREVISIAE;

FERMENTATION; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; MONOSACCHARIDE TRANSPORT PROTEINS; MUTATION, MISSENSE; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; XYLOSE;

EID: 85019889778     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00095-17     Document Type: Article

References (40)

1. Solomon BD. 2010. Biofuels and sustainability. Ann N Y Acad Sci 1185: 119-134. https://doi.org/10.1111/j.1749-6632.2009.05279.x.
2. Zaldivar J, Nielsen J, Olsson L. 2001. Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56:17-34.
3. Carroll A, Somerville C. 2009. Cellulosic biofuels. Annu Rev Plant Biol 60:165-182. https://doi.org/10.1146/annurev.arplant.043008.092125.
4. Kotter P, Ciriacy M. 1993. Xylose fermentation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 38:776-783. https://doi.org/10.1007/BF00167144.
5. Tantirungkij M, Seki T, Yoshida T. 1994. Genetic improvement of Saccharomyces cerevisiae for ethanol production from xylose. Ann N Y Acad Sci 721:138-147. https://doi.org/10.1111/j.1749-6632.1994.tb47386.x.
6. Kuyper M, Harhangi HR, Stave AK, Winkler AA, Jetten MS, de Laat WT, den Ridder JJ, Op den Camp HJ, van Dijken JP, Pronk JT. 2003. High-level functional expression of a fungal xylose isomerase: the key to efficient ethanolic fermentation of xylose by Saccharomyces cerevisiae? FEMS Yeast Res 4:69-78. https://doi.org/10.1016/S1567-1356(03)00141-7.
7. Kuyper M, Toirkens MJ, Diderich JA, Winkler AA, van Dijken JP, Pronk JT. 2005. Evolutionary engineering of mixed-sugar utilization by a xylosefermenting Saccharomyces cerevisiae strain. FEMS Yeast Res 5:925-934. https://doi.org/10.1016/j.femsyr.2005.04.004.
8. Kuyper M, Winkler AA, van Dijken JP, Pronk JT. 2004. Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: a proof of principle. FEMS Yeast Res 4:655-664. https://doi.org/10.1016/j.femsyr.2004.01.003.
9. Hamacher T, Becker J, Gardonyi M, Hahn-Hagerdal B, Boles E. 2002. Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 148(Pt 9):2783-2788. https://doi.org/10.1099/00221287-148-9-2783.
10. von Sivers M, Zacchi G, Olsson L, Hahn-Hagerdal B. 1994. Cost analysis of ethanol production from willow using recombinant Escherichia coli. Biotechnol Prog 10:555-560. https://doi.org/10.1021/bp00029a017.
11. Young EM, Comer AD, Huang H, Alper HS. 2012. A molecular transporter engineering approach to improving xylose catabolism in Saccharomyces cerevisiae. Metab Eng 14:401-411. https://doi.org/10.1016/j.ymben.2012.03.004.
12. Ren C, Chen T, Zhang J, Liang L, Lin Z. 2009. An evolved xylose transporter from Zymomonas mobilis enhances sugar transport in Escherichia coli. Microb Cell Fact 8:66. https://doi.org/10.1186/1475-2859-8-66.
13. Du J, Li S, Zhao H. 2010. Discovery and characterization of novel D-xylose-specific transporters from Neurospora crassa and Pichia stipitis. Mol Biosyst 6:2150-2156. https://doi.org/10.1039/c0mb00007h.
14. Hector RE, Qureshi N, Hughes SR, Cotta MA. 2008. Expression of a heterologous xylose transporter in a Saccharomyces cerevisiae strain engineered to utilize xylose improves aerobic xylose consumption. Appl Microbiol Biotechnol 80:675-684. https://doi.org/10.1007/s00253-008-1583-2.
15. Leandro MJ, Goncalves P, Spencer-Martins I. 2006. Two glucose/xylose transporter genes from the yeast Candida intermedia: first molecular characterization of a yeast xylose-H+ symporter. Biochem J 395: 543-549. https://doi.org/10.1042/BJ20051465.
16. Runquist D, Hahn-Hagerdal B, Radstrom P. 2010. Comparison of heterologous xylose transporters in recombinant Saccharomyces cerevisiae. Biotechnol Biofuels 3:5. https://doi.org/10.1186/1754-6834-3-5.
17. Farwick A, Bruder S, Schadeweg V, Oreb M, Boles E. Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose. Proc Natl Acad Sci U S A 111:5159-5164. https://doi.org/10.1073/pnas.1323464111.
18. Young EM, Tong A, Bui H, Spofford C, Alper HS. 2014. Rewiring yeast sugar transporter preference through modifying a conserved protein motif. Proc Natl Acad Sci U S A 111:131-136. https://doi.org/10.1073/pnas.1311970111.
19. Kruckeberg AL. 1996. The hexose transporter family of Saccharomyces cerevisiae. Arch Microbiol 166:283-292. https://doi.org/10.1007/s002030050385.
20. Boles E, Hollenberg CP. 1997. The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21:85-111. https://doi.org/10.1111/j.1574-6976.1997.tb00346.x.
21. Saloheimo A, Rauta J, Stasyk OV, Sibirny AA, Penttila M, Ruohonen L. 2007. Xylose transport studies with xylose-utilizing Saccharomyces cerevisiae strains expressing heterologous and homologous permeases. Appl Microbiol Biotechnol 74:1041-1052. https://doi.org/10.1007/s00253-006-0747-1.
22. Nijland JG, Shin HY, de Jong RM, de Waal PP, Klaassen P, Driessen AJ. 2014. Engineering of an endogenous hexose transporter into a specific D-xylose transporter facilitates glucose-xylose co-consumption in Saccharomyces cerevisiae. Biotechnol Biofuels 7:168. https://doi.org/10.1186/s13068-014-0168-9.
23. Reznicek O, Facey SJ, de Waal PP, Teunissen AWRH, de Bont JAM, Nijland JG, Driessen AJM, Hauer B. 2015. Improved xylose uptake in Saccharomyces cerevisiae due to directed evolution of galactose permease Gal2 for sugar co-consumption. J Appl Microbiol 119:99-111. https://doi.org/10.1111/jam.12825.
24. Nijkamp JF, van den Broek M, Datema E, de Kok S, Bosman L, Luttik MA, Daran-Lapujade P, Vongsangnak W, Nielsen J, Heijne WHM, Klaassen P, Paddon CJ, Platt D, Kötter P, van Ham RC, Reinders MJT, Pronk JT, de Ridder D, Daran J-M. 2012. De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microb Cell Fact 11:36. https://doi.org/10.1186/1475-2859-11-36.
25. Fleming AB, Beggs S, Church M, Tsukihashi Y, Pennings S. 2014. The yeast Cyc8-Tup1 complex cooperates with Hda1p and Rpd3p histone deacetylases to robustly repress transcription of the subtelomeric FLO1 gene. Biochim Biophys Acta 1839:1242-1255. https://doi.org/10.1016/j.bbagrm.2014.07.022.
26. Zha J, Shen M, Hu M, Song H, Yuan Y. 2014. Enhanced expression of genes involved in initial xylose metabolism and the oxidative pentose phosphate pathway in the improved xylose-utilizing Saccharomyces cerevisiae through evolutionary engineering. J Ind Microbiol Biotechnol 41:27-39. https://doi.org/10.1007/s10295-013-1350-y.
27. Tzamarias D, Struhl K. 1995. Distinct TPR motifs of Cyc8 are involved in recruiting the Cyc8-Tup1 corepressor complex to differentially regulated promoters. Genes Dev 9:821-831. https://doi.org/10.1101/gad.9.7.821.
28. Smith RL, Johnson AD. 2000. Turning genes off by Ssn6-Tup1: a conserved system of transcriptional repression in eukaryotes. Trends Biochem Sci 25:325-330. https://doi.org/10.1016/S0968-0004(00)01592-9.
29. Nehlin JO, Ronne H. 1990. Yeast MIG1 repressor is related to the mammalian early growth response and Wilms' tumour finger proteins. EMBO J 9:2891-2898.
30. Treitel MA, Carlson M. 1995. Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc Natl Acad Sci U S A 92: 3132-3136. https://doi.org/10.1073/pnas.92.8.3132.
31. DeRisi JL, Iyer VR, Brown PO. 1997. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278:680-686. https://doi.org/10.1126/science.278.5338.680.
32. Chujo M, Yoshida S, Ota A, Murata K, Kawai S. 2015. Acquisition of the ability to assimilate mannitol by Saccharomyces cerevisiae through dysfunction of the general corepressor Tup1-Cyc8. Appl Environ Microbiol 81:9-16. https://doi.org/10.1128/AEM.02906-14.
33. Lipke PN, Hull-Pillsbury C. 1984. Flocculation of Saccharomyces cerevisiae tup1 mutants. J Bacteriol 159:797-799.
34. Wong KH, Struhl K. 2011. The Cyc8-Tup1 complex inhibits transcription primarily by masking the activation domain of the recruiting protein. Genes Dev 25:2525-2539. https://doi.org/10.1101/gad.179275.111.
35. Jordan P, Choe J-Y, Boles E, Oreb M. 2016. Hxt13, Hxt15, Hxt16 and Hxt17 from Saccharomyces cerevisiae represent a novel type of polyol transporters. Sci Rep 6:23502. https://doi.org/10.1038/srep23502.
36. Toivari MH, Salusjärvi L, Ruohonen L, Penttilä M. 2004. Endogenous xylose pathway in Saccharomyces cerevisiae. Appl Environ Microbiol 70:3681-3686. https://doi.org/10.1128/AEM.70.6.3681-3686.2004.
37. Traff KL, Otero Cordero RR, van Zyl WH, Hahn-Hagerdal B. 2001. Deletion of the GRE3 aldose reductase gene and its influence on xylose metabolism in recombinant strains of Saccharomyces cerevisiae expressing the xylA and XKS1 genes. Appl Environ Microbiol 67:5668-5674. https://doi.org/10.1128/AEM.67.12.5668-5674.2001.
38. Shin HY, Nijland JG, de Waal PP, de Jong RM, Klaassen P, Driessen AJM. 2015. An engineered cryptic Hxt11 sugar transporter facilitates glucosexylose co-consumption in Saccharomyces cerevisiae. Biotechnol Biofuels 8:176. https://doi.org/10.1186/s13068-015-0360-6.
39. Luttik MA, Kötter P, Salomons FA, van der Klei IJ, van Dijken JP, Pronk JT. 2000. The Saccharomyces cerevisiae ICL2 gene encodes a mitochondrial 2-methylisocitrate lyase involved in propionyl-coenzyme A metabolism. J Bacteriol 182:7007-7013. https://doi.org/10.1128/JB.182.24.7007-7013.2000.
40. Mans R, van Rossum HM, Wijsman M, Backx A, Kuijpers NGA, van den Broek M, Daran-Lapujade P, Pronk JT, van Maris AJA, Daran J-MG. 2015. CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res 15:fov004-fov004. https://doi.org/10.1093/femsyr/fov004.