Laboratory evolution of a glucose-phosphorylation-deficient, arabinose-fermenting S. cerevisiae strain reveals mutations in GAL2 that enable glucose-insensitive l-arabinose uptake

FEMS Yeast Research

Volumn 18, Issue 6, 2018, Pages

  Verhoeven, Maarten D ^a   Bracher, Jasmine M ^a   Nijland, Jeroen G ^b   Bouwknegt, Jonna ^a   Daran, Jean Marc G ^a   Driessen, Arnold J M ^b   Van Maris, Antonius J A ^a,c   Pronk, Jack T ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c ALBANOVA UNIVERSITY CENTER   (Sweden)

Author keywords

Bioethanol; Gene duplication; L arabinose; Laboratory evolution; Pentose fermentation; Transporter engineering; Yeast

Indexed keywords

ARABINOSE; GALACTOSE; GLUCOSE; XYLOSE; GAL2 PROTEIN, S CEREVISIAE; GLUCOSE TRANSPORTER; SACCHAROMYCES CEREVISIAE PROTEIN;

ALLELE; ANAEROBIC GROWTH; ARTICLE; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; FUNGUS CULTURE; GAL2 GENE; GENE MUTATION; GLUCOSE TRANSPORT; NONHUMAN; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; WILD TYPE; DIRECTED MOLECULAR EVOLUTION; FERMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; MICROBIOLOGY; MUTATION; TRANSPORT AT THE CELLULAR LEVEL;

ANAEROBIOSIS; ARABINOSE; BIOLOGICAL TRANSPORT; DIRECTED MOLECULAR EVOLUTION; FERMENTATION; GLUCOSE; INDUSTRIAL MICROBIOLOGY; KINETICS; MONOSACCHARIDE TRANSPORT PROTEINS; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; XYLOSE;

EID: 85053495681     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1093/femsyr/foy062     Document Type: Article

References (67)

1. Ahuatzi D, Riera A, Peláez R et al. Hxk2 regulates the phosphorylation state of Mig1 and therefore its nucleocytoplasmic distribution. J Biol Chem 2007;282:4485–93.
2. Bakker BM, Overkamp KM, van Maris AJ et al. Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol Rev 2001;25:15–37.
3. Becker J, Boles E. A modified Saccharomyces cerevisiae strain that consumes L-arabinose and produces ethanol. Appl Environ Microbiol 2003;69:4144–50.
4. Biswas C, Djordjevic JT, Zuo X et al. Functional characterization of the hexose transporter Hxt13p: an efflux pump that mediates resistance to miltefosine in yeast. Fungal Gene Biol 2013;61:23–32.
5. Boender LG, de Hulster EA, van Maris AJ et al. Quantitative physiology of Saccharomyces cerevisiae at near-zero specific growth rates. Appl Environ Microbiol 2009;75:5607–14.
6. Bracher JM, Verhoeven MD, Wisselink HW et al. The Penicillium chrysogenum transporter PcAraT enables high-affinity, glucose-insensitive l-arabinose transport in Saccharomyces cerevisiae. Biotechnol Biofuels 2018;11:63.
7. Bro C, Knudsen S, Regenberg B et al. Improvement of galactose uptake in Saccharomyces cerevisiae through overexpression of phosphoglucomutase: example of transcript analysis as a tool in inverse metabolic engineering. Appl Environ Microbiol 2005;71:6465–72.
8. Crowley JH, Leak FW, Shianna KV et al. A mutation in a purported regulatory gene affects control of sterol uptake in Saccharomyces cerevisiae. J Bacteriol 1998;180:4177–83.
9. DiCarlo JE, Norville JE, Mali P et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 2013;41:4336–43.
10. Dickson RC, Nagiec EE, Wells GB et al. Synthesis of mannose-(inositol-P) 2-ceramide, the major sphingolipid in Saccharomyces cerevisiae, requires the IPT1 (YDR072c) gene. J Biol Chem 1997;272:29620–5.
11. Entian K-D, Kötter P. 25 Yeast genetic strain and plasmid collections. Method Microbiol 2007;36:629–66.
12. Farwick A, Bruder S, Schadeweg V et al. Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose. Proc Natl Acad Sci 2014;111:5159–64.
13. Gietz RD, Schiestl RH, Willems AR et al. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1995;11:355–360.
14. Gorter de Vries AR, Pronk JT, Daran J-MG. Industrial relevance of chromosomal copy number variation in Saccharomyces yeasts. Appl Environ Microbiol 2017;83:e03206–03216.
15. Grohmann K, Bothast RJ. Pectin-rich residues generated by processing of citrus fruits, apples, and sugar beets. ACS Symposium Series 1994;566:372390. 1994;566:372–390.
16. Grohmann K, Bothast RJ. Saccharification of corn fibre by combined treatment with dilute sulphuric acid and enzymes. Process Biochem 1997;32:405–15.
17. Guadalupe Medina V, Almering MJ, van Maris AJ et al. Elimination of glycerol production in anaerobic cultures of a Saccharomyces cerevisiae strain engineered to use acetic acid as an electron acceptor. Appl Environ Microbiol 2010;76:190–5.
18. Hamacher T, Becker J, Gárdonyi M et al. Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 2002;148:2783–8.
19. Jeffries TW. Utilization of xylose by bacteria, yeasts, and fungi. Pentoses and Lignin, Springer, Berlin, Heidelberg, 1983; pp. 1–32.
20. Jordan P, Choe J-Y, Boles E et al. Hxt13, Hxt15, Hxt16 and Hxt17 from Saccharomyces cerevisiae represent a novel type of polyol transporters. Sci Rep 2016:6:23502.
21. Knoshaug EP, Vidgren V, Magalhães F et al. Novel transporters from Kluyveromyces marxianus and Pichia guilliermondii expressed in Saccharomyces cerevisiae enable growth on l-arabinose and d-xylose. Yeast 2015;32:615–28.
22. Kou S-C, Christensen MS, Cirillo VP. Galactose transport in Saccharomyces cerevisiae II. Characteristics of galactose uptake and exchange in galactokinaseless cells. J Bacteriol 1970;103:671–8.
23. Kuijpers NG, Chroumpi S, Vos T et al. One-step assembly and targeted integration of multigene constructs assisted by the I-SceI meganuclease in Saccharomyces cerevisiae. FEMS Yeast Res 2013;13:769–81.
24. Kuyper M, Hartog MM, Toirkens MJ et al. Metabolic engineering of a xylose-isomerase-expressing strain for rapid anaerobic xylose fermentation. FEMS Yeast Res 2005;5:399–409.
25. Kuyper M, Harhangi HR, Stave AK et al. High-level functional expression of a fungal xylose isomerase: the key to efficient ethanolic fermentation of xylose by Saccharomyces cerevisiae. FEMS Yeast Res 2003;4:69–78.
26. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25:1754–60.
27. Li J, Xu J, Cai P et al. Functional analysis of two L-arabinose transporters from filamentous fungi reveals promising characteristics for improved pentose utilization in Saccharomyces cerevisiae. Appl Environ Microbiol 2015;81:4062–70.
28. Lynd LR. Overview and evaluation of fuel ethanol from cellulosic biomass: technology, economics, the environment, and policy. Annu Rev Energy Environ 1996;21:403–65.
29. Mans R, van Rossum HM, Wijsman M et al. CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res 2015;15:fov004.
30. Nijkamp JF, van den Broek MA, Geertman JMA et al. De novo detection of copy number variation by co-assembly. Bioinformatics 2012;28:3195–202.
31. Nijkamp JF, van den Broek M, Datema E et al. 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 2012;11:36.
32. Nijland JG, Shin HY, de Jong RM et al. Engineering of an endogenous hexose transporter into a specific D-xylose transporter facilitates glucose-xylose co-consumption in Saccharomyces cerevisiae. Biotechnol Biofuels 2014;7:168.
33. Ostergaard S, Walløe KO, Gomes CS et al. The impact of GAL6, GAL80, and MIG1 on glucose control of the GAL system in Saccharomyces cerevisiae. FEMS Yeast Res 2001;1:47–55.
34. Oud B, van Maris AJ, Daran J-M et al. Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast. FEMS Yeast Res 2012;12:183–96.
35. Raamsdonk LM, Diderich JA, Kuiper A et al. Co-consumption of sugars or ethanol and glucose in a Saccharomyces cerevisiae strain deleted in the HXK2 gene. Yeast 2001;18:1023–33.
36. Reifenberger E, Boles E, Ciriacy M. Kinetic characterization of individual hexose transporters of Saccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. FEBS J 1997;245:324–33.
37. Renewable Fuels Association. World fuel ethanol, 2017; production.available at: http://ethanolrfa.org/resources/industry/statistics/.
38. Richard P, Putkonen M, Väänänen R et al. The missing link in the fungal L-arabinose catabolic pathway, identification of the L-xylulose reductase gene. Biochemistry 2002;41:6432–7.
39. Roberts RL, Mösch H-U, Fink GR. 14-3-3 proteins are essential for RAS/MAPK cascade signaling during pseudohyphal development in S. cerevisiae. Cell 1997;89:1055–65.
40. Sedlak M, Ho NW. Expression of E. coli araBAD operon encoding enzymes for metabolizing L-arabinose in Saccharomyces cerevisiae. Enzyme Microb Technol 2001;28:16–24.
41. Solis-Escalante D, Kuijpers NG, Barrajon-Simancas N et al. A minimal set of glycolytic genes reveals strong redundancies in Saccharomyces cerevisiae central metabolism. Eukaryotic Cell 2015;14:804–16.
42. Solis-Escalante D, Kuijpers NG, Bongaerts N et al. amdSYM, a new dominant recyclable marker cassette for Saccharomyces cerevisiae. FEMS Yeast Res 2013;13:126–39.
43. Subtil T, Boles E. Improving L-arabinose utilization of pentose fermenting Saccharomyces cerevisiae cells by heterologous expression of L-arabinose transporting sugar transporters. Biotechnol Biofuels 2011;4:38.
44. Subtil T, Boles E. Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnol Biofuels 2012;5:14.
45. Sun L, Zeng X, Yan C et al. Crystal structure of a bacterial homologue of glucose transporters GLUT1-4. Nature 2012;490:361–6.
46. Tani T, Taguchi H, Fujimori KE et al. Isolation and characterization of xylitol-assimilating mutants of recombinant Saccharomyces cerevisiae. J Biosci Bioeng 2016;122:446–55.
47. Thorvaldsdóttir H, Robinson JT, Mesirov JP. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Briefings in Bioinformatics 2013;14:178–92.
48. Torchia T, Hamilton R, Cano C et al. Disruption of regulatory gene GAL80 in Saccharomyces cerevisiae: effects on carbon-controlled regulation of the galactose/melibiose pathway genes. Mol Cell Biol 1984;4:1521–7.
49. Träff K, Cordero RO, Van Zyl W et al. 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 2001;67: 5668–74.
50. Tsai C-S, Kong II, Lesmana A et al. Rapid and marker-free refac-toring of xylose-fermenting yeast strains with Cas9/CRISPR. Biotechnol Bioeng 2015;112:2406–11.
51. Van Hemert M, van Heusden G, Steensma H. Yeast 14-3-3 proteins. Yeast 2001;18:889–95.
52. van Heusden GPH, Wenzel TJ, Lagendijk EL et al. Characterization of the yeast BMH1 gene encoding a putative protein homologous to mammalian protein kinase II activators and protein kinase C inhibitors. FEBS Lett 1992;302:145–50.
53. van Maris AJ, Abbott DA, Bellissimi E et al. Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Antonie van Leeuwenhoek 2006;90:391–418.
54. Verduyn C, Postma E, Scheffers WA et al. Physiology of Saccharomyces cerevisiae in Anaerobic Glucose-Limited Chemostat Cultures. Microbiology 1990;136:395–403.
55. Verduyn C, Postma E, Scheffers WA et al. Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 1992;8:501–17.
56. Verho R, Penttilä M, Richard P. Cloning of two genes (LAT1,2) encoding specific l-arabinose transporters of the l-arabinose fermenting yeast Ambrosiozyma monospora. Appl Biochem Biotechnol 2011;164:604–11.
57. Verhoeven MD, Lee M, Kamoen L et al. Mutations in PMR1 stimulate xylose isomerase activity and anaerobic growth on xylose of engineered Saccharomyces cerevisiae by influencing manganese homeostasis. Sci Rep 2017;7: 46155.
58. Walker BJ, Abeel T, Shea T et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 2014;9:e112963.
59. Wang C, Skinner C, Easlon E et al. Deleting the 14-3-3 protein Bmh1 extends life span in Saccharomyces cerevisiae by increasing stress response. Genetics 2009;183: 1373–84.
60. Wang C, Shen Y, Zhang Y et al. Improvement of L-arabinose fermentation by modifying the metabolic pathway and transport in Saccharomyces cerevisiae. BioMed Research International 2013;2013:461204.
61. Wang C, Li Y, Qiu C et al. Identification of important amino acids in Gal2p for improving the l-arabinose transport and metabolism in Saccharomyces cerevisiae. Front Microbiol 2017;8:1391.
62. Weusthuis RA, Pronk JT, Van Den Broek P et al. Chemostat cultivation as a tool for studies on sugar transport in yeasts. Microbiol Rev 1994;58:1–9.
63. Wiedemann B, Boles E. Codon-optimized bacterial genes improve L-arabinose fermentation in recombinant Saccharomyces cerevisiae. Appl Environ Microbiol 2008;74:2043–50.
64. Wisselink HW, Toirkens MJ, Wu Q et al. Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 2009;75:907–14.
65. Wisselink HW, Van Maris AJA, Pronk JT et al. Polypeptides with permease activity. US Patent 9034608 B2, 2015.
66. Wisselink HW, Toirkens MJ, Del Rosario Franco Berriel M et al. Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of l-arabinose. Appl Environ Microbiol 2007;73:4881–91.
67. Wisselink HW, Cipollina C, Oud B et al. Metabolome, tran-scriptome and metabolic flux analysis of arabinose fermentation by engineered Saccharomyces cerevisiae. Metab Eng 2010;12:537–51.