Increased xylose affinity of Hxt2 through gene shuffling of hexose transporters in Saccharomyces cerevisiae

Journal of Applied Microbiology

Volumn 124, Issue 2, 2018, Pages 503-510

  Nijland, J G ^a   Shin, H Y ^a   de Waal, P P ^b   Klaassen, P ^b   Driessen, A J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b DSM BIOTECHNOLOGY CENTER   (Netherlands)

Author keywords

biofuels; biotechnology; fermentation; metabolism; transport; xylose; yeast

Indexed keywords

AMINO ACIDS; BIOETHANOL; ETHANOL; GENES; PROTEINS; XYLOSE;

BIO-ETHANOL PRODUCTION; CELLULOSIC MATERIAL; D-XYLOSE; FUSION PROTEINS; GENE SHUFFLING; HEXOSE TRANSPORTERS; LOW CONCENTRATIONS; PROTEIN FUSION; TRANSPORT; XYLOSE TRANSPORT;

YEAST;

CHIMERIC PROTEIN; CYSTEINE; GLUCOSE TRANSPORTER; PROLINE; XYLOSE; CARRIER PROTEIN; GLUCOSE; HXT2 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

BIOFUEL; BIOTECHNOLOGY; CONCENTRATION (COMPOSITION); ETHANOL; FERMENTATION; GENE; METABOLISM; PROTEIN; SUGAR; TRANSPORT PROCESS; YEAST;

ARTICLE; CONTROLLED STUDY; DNA SHUFFLING; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE MUTATION; MOLECULAR LIBRARY; NONHUMAN; SACCHAROMYCES CEREVISIAE; GENETICS; METABOLISM; MISSENSE MUTATION; TRANSPORT AT THE CELLULAR LEVEL;

SACCHAROMYCES CEREVISIAE;

BIOLOGICAL TRANSPORT; DNA SHUFFLING; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; MEMBRANE TRANSPORT PROTEINS; MUTATION, MISSENSE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; XYLOSE;

EID: 85040821685     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13670     Document Type: Article

References (33)

1. Boles, E. and Hollenberg, C.P. (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21, 85–111.
2. Carroll, A. and Somerville, C. (2009) Cellulosic biofuels. Annu Rev Plant Biol 60, 165–182.
3. Cornish-Bowden, A. and Eisenthal, R. (1974) Statistical considerations in the estimation of enzyme kinetic parameters by the direct linear plot and other methods. Biochem J 139, 721–730.
4. Du, J., Li, S. and Zhao, H. (2010) Discovery and characterization of novel d-xylose-specific transporters from Neurospora crassa and Pichia stipitis. Mol BioSyst 6, 2150–2156.
5. Eisenthal, R. and Cornish-Bowden, A. (1974) The direct linear plot. A new graphical procedure for estimating enzyme kinetic parameters. Biochem J 139, 715–720.
6. Farwick, A., Bruder, S., Schadeweg, V., Oreb, M. and Boles, E. (2014) Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose. Proc Natl Acad Sci USA 111, 5159–5164.
7. Gírio, F.M., Fonseca, C., Carvalheiro, F., Duarte, L.C., Marques, S. and Bogel-Łukasik, R. (2010) Hemicelluloses for fuel ethanol: a review. Bioresour Technol 101, 4775–4800.
8. Gonçalves, D.L., Matsushika, A., de Sales, B.B., Goshima, T., Bon, E.P.S. and Stambuk, B.U. (2014) Xylose and xylose/glucose co-fermentation by recombinant Saccharomyces cerevisiae strains expressing individual hexose transporters. Enzyme Microb Technol 63, 13–20.
9. Hamacher, T., Becker, J., Gardonyi, M., Hahn-Hagerdal, B. and Boles, E. (2002a) Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 148, 2783–2788.
10. Hamacher, T., Becker, J., Gárdonyi, M., Hahn-Hägerdal, B. and Boles, E. (2002b) Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 148, 2783–2788.
11. Kasahara, T. and Kasahara, M. (2003) Transmembrane segments 1, 5, 7 and 8 are required for high-affinity glucose transport by Saccharomyces cerevisiae Hxt2 transporter. Biochem J 372, 247–252.
12. Kasahara, T. and Kasahara, M. (2010) Identification of a key residue determining substrate affinity in the yeast glucose transporter Hxt7: a two-dimensional comprehensive study. J Biol Chem 285, 26263–26268.
13. Kasahara, T., Ishiguro, M. and Kasahara, M. (2004) Comprehensive chimeric analysis of amino acid residues critical for high affinity glucose transport by Hxt2 of Saccharomyces cerevisiae. J Biol Chem 279, 30274–30278.
14. Kasahara, T., Ishiguro, M. and Kasahara, M. (2006) Eight amino acid residues in transmembrane segments of yeast glucose transporter Hxt2 are required for high affinity transport. J Biol Chem 281, 18532–18538.
15. Kasahara, T., Maeda, M., Ishiguro, M. and Kasahara, M. (2007) Identification by comprehensive chimeric analysis of a key residue responsible for high affinity glucose transport by yeast HXT2. J Biol Chem 282, 13146–13150.
16. Kasahara, T., Maeda, M., Boles, E. and Kasahara, M. (2009) Identification of a key residue determining substrate affinity in the human glucose transporter GLUT1. Biochim Biophys Acta 1788, 1051–1055.
17. Kasahara, T., Shimogawara, K. and Kasahara, M. (2011) Crucial effects of amino acid side chain length in transmembrane segment 5 on substrate affinity in yeast glucose transporter Hxt7. Biochemistry 50, 8674–8681.
18. Kotter, P. and Ciriacy, M. (1993) Xylose fermentation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 38, 776–783.
19. Kuyper, M., Winkler, A.A., van Dijken, J.P. and Pronk, J.T. (2004) Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: a proof of principle. FEMS Yeast Res 4, 655–664.
20. Li, H., Schmitz, O. and Alper, H.S. (2016) Enabling glucose/xylose co-transport in yeast through the directed evolution of a sugar transporter. Appl Microbiol Biotechnol 100, 10215–10223.
21. Maier, A., Völker, B., Boles, E. and Fuhrmann, G.F. (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.
22. Nijland, J.G., Shin, H.Y., de Jong, R.M., de Waal, P.P., Klaassen, P. and Driessen, A.J. (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.
23. Reifenberger, E., Boles, E. and 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.
24. Reznicek, O., Facey, S.J., de Waal, P.P., Teunissen, A.W.R.H., de Bont, J.A.M., Nijland, J.G., Driessen, A.J.M. and 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.
25. Saloheimo, A., Rauta, J., Stasyk, O.V., Sibirny, A.A., Penttila, M. and Ruohonen, L. (2007) Xylose transport studies with xylose-utilizing Saccharomyces cerevisiae strains expressing heterologous and homologous permeases. Appl Microbiol Biotechnol 74, 1041–1052.
26. Sedlak, M. and Ho, N.W.Y. (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.
27. Shin, H.Y., Nijland, J.G., de Waal, P.P., de Jong, R.M., Klaassen, P. and Driessen, A.J.M. (2015) An engineered cryptic Hxt11 sugar transporter facilitates glucose–xylose co-consumption in Saccharomyces cerevisiae. Biotechnol Biofuels 8, 176.
28. Shin, H.Y., Nijland, J.G., de Waal, P.P. and Driessen, A.J.M. (2017) The amino-terminal tail of Hxt11 confers membrane stability to the Hxt2 sugar transporter and improves Xylose fermentation in the presence of acetic acid. Biotechnol Bioeng.
29. Solomon, B.D. (2010) Biofuels and sustainability. Ann N Y Acad Sci 1185, 119–134.
30. Stemmer, W.P. (1994) DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc Natl Acad Sci USA 91, 10747–10751.
31. Van Maris, A.J.A., Winkler, A.A., Kuyper, M., De Laat, W.T.A.M., Van Dijken, J.P. and Pronk, J.T. (2007) Development of efficient xylose fermentation in Saccharomyces cerevisiae: xylose isomerase as a key component. Adv Biochem Eng 108, 179–204.
32. Young, E.M., Comer, A.D., Huang, H. and Alper, H.S. (2012) A molecular transporter engineering approach to improving xylose catabolism in Saccharomyces cerevisiae. Metab Eng 14, 401–411.
33. Young, E.M., Tong, A., Bui, H., Spofford, C. and Alper, H.S. (2014) Rewiring yeast sugar transporter preference through modifying a conserved protein motif. Proc Natl Acad Sci USA 111, 131–136.