Novel transporters from Kluyveromyces marxianus and Pichia guilliermondii expressed in Saccharomyces cerevisiae enable growth on l-arabinose and d-xylose

Yeast

Volumn 32, Issue 10, 2015, Pages 615-628

  Knoshaug, Eric P ^a   Vidgren, Virve ^b   Magalhães, Frederico ^b   Jarvis, Eric E ^a   Franden, Mary Ann ^a   Zhang, Min ^a   Singh, Arjun ^a  

^a NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

^b VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

Author keywords

arabinose; GAL2; transport; xylose; yeast

Indexed keywords

ARABINOSE; GAL2P PROTEIN; GALACTOSE; GENOMIC DNA; GLUCOSE TRANSPORTER; HEXOSE; KMAXT1P PROTEIN; PENTOSE; PGAXT1 TRANSPORTER PROTEIN; PROTEIN; UNCLASSIFIED DRUG; XYLOSE; CARRIER PROTEIN; FUNGAL PROTEIN;

ARTICLE; DIFFERENTIAL DISPLAY; ELECTROTRANSFORMATION; FUNGAL GENETICS; FUNGAL STRAIN; GENE EXPRESSION; GENETIC CODE; GROWTH CURVE; HEXOSE TRANSPORT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; KLUYVEROMYCES MARXIANUS; MEYEROZYMA GUILLIERMONDII; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS; TRANSPORT ASSAY; TRANSPORT KINETICS; CHEMISTRY; GENETIC ENGINEERING; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; KLUYVEROMYCES; METABOLISM; PICHIA; TRANSPORT AT THE CELLULAR LEVEL;

ARABINOSE; BIOLOGICAL TRANSPORT; FUNGAL PROTEINS; GENE EXPRESSION; GENETIC ENGINEERING; KINETICS; KLUYVEROMYCES; MEMBRANE TRANSPORT PROTEINS; PICHIA; SACCHAROMYCES CEREVISIAE; XYLOSE;

EID: 84965185990     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.3084     Document Type: Article

References (64)

1. Alves-Araujo C, Hernandez-Lopez MJ, Sousa MJ, et al. 2004. Cloning and characterization of the MAL11 gene encoding a high-affinity maltose transporter from Torulaspora delbrueckii. FEMS Yeast Res 4: 467–476.
2. Becker J, Boles E. 2003. A modified Saccharomyces cerevisiae strain that consumes l-arabinose and produces ethanol. Appl Environ Microbiol 69: 4144–4150.
3. Bera A, Sedlak M, Khan A, Ho N. 2010. Establishment of l-arabinose fermentation in glucose/xylose co-fermenting recombinant Saccharomyces cerevisiae 424A(LNH-ST) by genetic engineering. Appl Biochem Biotechnol 87: 1803–1811.
4. Bettiga M, Bengtsson O, Hahn-Hagerdal B, Gorwa-Grauslund M. 2009. Arabinose and xylose fermentation by recombinant Saccharomyces cerevisiae expressing a fungal pentose utilization pathway. Microb Cell Fact 8: 40.
5. Bisson LF, Fraenkel DG. 1984. Expression of kinase-dependent glucose uptake in Saccharomyces cerevisiae. J Bacteriol 159: 1013–1017.
6. Brat D, Boles E, Wiedemann B. 2009. Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl Environ Microbiol 75: 2304–2311.
7. Cirillo VP. 1968. Galactose Transport in Saccharomyces cerevisiae I. Non-metabolized sugars as substrates and inducers of the galactose transport system. J Bacteriol 95: 1727–1731.
8. Davis R, Tao L, Tan ECD, et al. 2013. Process design and economics for the conversion of lignocellulosic biomass to hydrocarbons: dilute acid and enzymatic deconstruction of biomass to sugars and biological conversion of sugars to hydrocarbons. NREL/TP-5100-60223.
9. Day RE, Higgins VJ, Rogers PJ, Dawes IW. 2002. Characterization of the putative maltose transporters encoded by YDL247w and YJR160c. Yeast 19: 1015–1027.
10. de Figueiredo Vilela L, de Mello VM, Reis VCB, et al. 2013. Functional expression of Burkholderia cenocepacia xylose isomerase in yeast increases ethanol production from a glucose–xylose blend. Bioresource Technol 128: 792–796.
11. Demeke MM, Dietz H, Li Y, et al. 2013. 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 Biofuel 6: 89.
12. Dien BS, Kurtzman CP, Saha BC, Bothast RJ. 1996. Screening for l-arabinose fermenting yeasts. Appl Biochem Biotechnol 57/58: 233–242.
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.
14. Dujon B, Sherman D, Fischer G, et al. 2004. Genome evolution in yeasts. Nature 430: 35–44.
15. Elbing K, Larsson C, Bill RM, et al. 2004. Role of hexose transport in control of glycolytic flux in Saccharomyces cerevisiae. Appl Environ Microbiol 70: 5323–5330.
16. Farwick A, Bruder S, Schadeweg V, et al. 2014. Engineering of yeast hexose transporters to transport d-xylose without inhibition by d-glucose. Proc Natl Acad Sci U S A 111: 5159–5164.
17. + symporter from the highly related yeast species Debaryomyces fabryi and Debaryomyces hansenii. FEMS Yeast Res 13: 585–596.
18. Gardonyi M, Jeppsson M, Liden G, et al. 2003. Control of xylose consumption by xylose transport in recombinant Saccharomyces cerevisiae. Biotechnol Bioeng 82: 818–824.
19. Goffrini P, Ferrero I, Donnini C. 2002. Respiration-dependent utilization of sugars in yeasts: a determinant role for sugar transporters. J Bacteriol 184: 427–432.
20. Hamacher T, Becker J, Gardonyi M, et al. 2002. Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 148: 2783–2788.
21. Hill J, Ian KA, Donald G, Griffiths DE. 1991. DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res 19: 5791.
22. Hofmann K, Stoffel W. 1993. A database of membrane spanning proteins segments. Biol Chem 374: 166.
23. Huibregtse JM, Good PD, Marczynski GT, et al. 1993. Gal4 protein binding is required but not sufficient for derepression and induction of GAL2 expression. J Biol Chem 268: 22,219–22,222.
24. Humbird D, Davis R, Tao L, et al. 2011. Process design and economics for biochemical conversion of lignocellulosic biomass to ethanol: dilute-acid pretreatment and enzymatic hydrolysis of corn stover. NREL/TP-5100-47764.
25. Karhumaa K, Wiedemann B, Hahn-Hagerdal B, et al. 2006. Co-utilization of l-arabinose and d-xylose by laboratory and industrial Saccharomyces cerevisiae strains. Microb Cell Fact 5: 8.
26. 504 in the yeast Gal2 transporter. FEBS Lett 471: 103–107.
27. Knoshaug EP, Franden MA, Stambuk BU, et al. 2009. Utilization and transport of l-arabinose by non-Saccharomyces yeasts. Cellulose 16: 729–741.
28. Kou SC, Christensen MS, Cirillo VP. 1970. Galactose transport in Saccharomyces cerevisiae II. Characteristics of galactose uptake and exchange in galactokinaseless cells. J Bacteriol 103: 671–678.
29. Kruckeberg AL. 1996. The hexose transporter family of Saccharomyces cerevisiae. Arch Microbiol 166: 283–292.
30. Kurtzman CP, Dien BS. 1998. Candida arabinofermentans, a new l-arabinose fermenting yeast. Antonie Van Leeuwenhoek 74: 237–243.
31. Leandro MJ, Fonseca C, Goncalves P. 2009. Hexose and pentose transport in ascomycetous yeasts: an overview. FEMS Yeast Res 9: 511–525.
32. + symporter. Biochem J 395: 543–549.
33. Lee WJ, Kim MD, Ryu YW, et al. 2002. Kinetic studies on glucose and xylose transport in Saccharomyces cerevisiae. Appl Biochem Biotechnol 60: 186–191.
34. 13C) xylose metabolism in Pichia stipitis under aerobic and anaerobic conditions. Appl Microbiol Biotechnol 28: 293–296.
35. Londesborough J, Richard P, Valkonen M, Viljanen K. 2014. Effect of C-terminal protein tags on pentitol and l-arabinose transport by Ambrosiozyma monospora Lat1 and Lat2 transporters in Sacccharmyces cerevisiae. Appl Environ Microbiol 80: 2737–2745.
36. Lucero P, Penalver E, Moreno E, Lagunas R. 1997. Moderate concentrations of ethanol inhibit endocytosis of the yeast maltose transporter. Appl Environ Microbiol 63: 3831–3836.
37. Maier A, Volker B, Boles E, Fuhrmann GF. 2002. Characterisation of glucose transport in Saccharomyces cerevisiae with plasma membrane vesicles (countertransport) and intact cells (initial uptake) with single Hxt1, Hxt2, Hxt3, Hxt4, Hxt6, Hxt7 or Gal2 transporters. FEMS Yeast Res 2: 539–550.
38. Menon V, Rao M. 2012. Trends in bioconversion of lignocellulose: biofuels, platform chemicals and biorefinery concept. Progr Energ Combust Sci 38: 522–550.
39. Mumberg D, Muller R, Funk M. 1995. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156: 119–122.
40. Nacken V, Achstetter T, Degryse E. 1996. Probing the limits of expression levels by varying promoter strength and plasmid copy number in Saccharomyces cerevisiae. Gene 175: 253–260.
41. Otterstedt K, Larsson C, Bill RM, et al. 2004. Switching the mode of metabolism in the yeast Saccharomyces cerevisiae. EMBO Rep 5: 532–537.
42. Pina C, Goncalves P, Prista C, Loureiro-Dias MC. 2004. Ffz1, a new transporter specific for fructose from Zygosaccharomyces bailii. Microbiology 150: 2429–2433.
43. Reifenberger E, Boles E, Ciriacy M. 1997. Kinetic characterization of individual hexose transporters of Saccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. Eur J Biochem 245: 324–333.
44. Richard P, Verho R, Putkonen M, et al. 2003. Production of ethanol from l-arabinose by Saccharomyces cerevisiae containing a fungal l-arabinose pathway. FEMS Yeast Res 3: 185–189.
45. Runquist D, Fonseca C, Radstrom P, et al. 2009. Expression of the Gxf1 transporter from Candida intermedia improves fermentation performance in recombinant xylose-utilizing Saccharomyces cerevisiae. Appl Microbiol Biotechnol 82: 123–130.
46. Saloheimo A, Rauta J, Stasyk OV, et al. 2007. Xylose transport studies with xylose-utilizing Saccharomyces cerevisiae strains expressing heterologous and homologous permeases. Appl Genet Mol Biotechnol 74: 1041–1052.
47. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY.
48. Sanchez RG, Karhumaa K, Fonseca C, et al. 2010. Improved xylose and arabinose utilization by an industrial recombinant Sacccharomyces cerevisiae strain using evolutionary engineering. Biotechnol Biofuel 3: 13.
49. Sedlak M, Ho NWY. 2001. Expression of E. coli araBAD operon encoding enzymes for metabolizing l-arabinose in Saccharomyces cerevisiae. Enzyme Microb Technol 28: 16–24.
50. Sedlak M, Ho NWY. 2004. Characterization of the effectiveness of hexose transporters for transporting xylose during glucose and xylose co-fermentation by a recombinant Saccharomyces yeast. Yeast 21: 671–684.
51. Stambuk BU, Franden MA, Singh A, Zhang M. 2003. d-Xylose transport by Candida succiphila and Kluyveromyces marxianus. Appl Biochem Biotechnol 105–108: 255–263.
52. Subtil T, Boles E. 2011. Improving L-arabinose utilization of pentose fermenting Saccharomyces cerevisiae cells by heterologous expression of l-arabinose transporting sugar transporters. Biotechnol Biofuels 4: 38.
53. Subtil T, Boles E. 2012. Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnol Biofuel 5: 14.
54. Sugita T, Nakase T. 1999. Non-universal usage of the leucine CUG codon in yeasts: investigation of basidiomycetous yeast. J Gen Appl Microbiol 45: 193–197.
55. Tschopp JF, Emr SD, Field C, et al. 1986. GAL2 codes for a membrane-bound subunit of the galactose permease in Saccharomyces cerevisiae. J Bacteriol 166: 313–318.
56. Tuite MF, Santos MAS. 1996. Codon reassignment in Candida species: an evolutionary conundrum. Biochimie 78: 993–998.
57. Verho R, Penttila M, Richard P. 2011. Cloning of two genes (LAT1, 2) encoding specific l-arabinose transporters of the l-arabinose fermenting yeast Ambrosiozyma monospora. Appl Biochem Biotechnol 164: 604–611.
58. Wang C, Shen Y, Zhang Y, et al. 2013. Improvement of l-arabinose fermentation by modifying the metabolic pathway and transport in Saccharomyces cerevisiae. BioMed Res Int 2013: 461204.
59. Weierstall T, Hollenberg CP, Boles E. 1999. Cloning and characterization of three genes (SUT1–3) encoding glucose transporters of the yeast Pichia stipitis. Mol Microbiol 31: 871–883.
60. Wendell DL, Bisson LF. 1994. Expression of high-affinity glucose transport protein Hxt2p of Saccharomyces cerevisiae is both repressed and induced by glucose and appears to be regulated posttranslationally. J Bacteriol 176: 3730–3737.
61. Wisselink HW, Cipollina C, Oud B, et al. 2010. Metabolome, transcriptome and metabolic flux analysis of arabinose fermentation by engineered Saccharomyces cerevisiae. Metab Eng 12: 537–551.
62. Young E, Lee SM, Alper H. 2010. Optimizing pentose utilization in yeast: the need for novel tools and approaches. Biotechnol Biofuel 3: 24.
63. Young E, Poucher A, Comer A, et al. 2011. Functional survey for heterologous sugar transport proteins, using Saccharomyces cerevisiae as a host. Appl Environ Microbiol 77: 3311–3319.
64. Young EM, Tong A, Bui H, et al. 2014. Rewiring yeast sugar transporter preference through modifying a conserved protein motif. Proc Natl Acad Sci U S A 111: 131–136.