Elimination of sucrose transport and hydrolysis in Saccharomyces cerevisiae: A platform strain for engineering sucrose metabolism

FEMS Yeast Research

Volumn 17, Issue 1, 2017, Pages

  Marques, Wesley Leoricy ^a,b   Mans, Robert ^a   Marella, Eko Roy ^a   Cordeiro, Rosa Lorizolla ^b   van den Broek, Marcel ^a   Daran, Jean Marc G ^a   Pronk, Jack T ^a   Gombert, Andreas K ^b   van Maris, Antonius J A ^a,c  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c ALBANOVA UNIVERSITY CENTER   (Sweden)

Author keywords

Disaccharide; Isomaltase; Laboratory evolution; Multiple gene deletion; Real time PCR; Reverse engineering

Indexed keywords

OLIGO 1,6 GLUCOSIDASE; SUCROSE;

ARTICLE; DNA PURIFICATION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE DELETION; GENETIC ENGINEERING; GLUCOSE ASSAY; GROWTH RATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; IN VITRO STUDY; METABOLIC ENGINEERING; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SANGER SEQUENCING; SUCROSE METABOLISM; WHOLE GENOME SEQUENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; GENE DELETION; HYDROLYSIS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; SACCHAROMYCES CEREVISIAE; SUCROSE;

EID: 85026699949     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1093/femsyr/fox006     Document Type: Article

References (61)

1. Alamäe T, Pärn P, Viigand K et al. Regulation of the Hansenula polymorpha maltase gene promoter in H. polymorpha and Saccharomyces cerevisiae. FEMS Yeast Res 2003;4:165-73
2. Alves SL, Herberts RA, Hollatz C et al. Molecular analysis of maltotriose active transport and fermentation by Saccharomyces cerevisiae reveals a determinant role for the AGT1 permease. Appl Environ Microb 2008;74:1494-501
3. Badotti F, Dário MG, Alves SL et al. Switching the mode of sucrose utilization by Saccharomyces cerevisiae. Microb Cell Fact 2008;7:4
4. Bali M, Zhang B, Morano KA et al. The Hsp90 molecular chaperone complex regulates maltose induction and stability of the Saccharomyces MAL gene transcription activator Mal63p. J Biol Chem 2003;278:47441-8
5. Basso TO, de Kok S, Dario M et al. Engineering topology and kinetics of sucrose metabolism in Saccharomyces cerevisiae for improved ethanol yield. Metab Eng 2011;13:694-703
6. Boeke JD, La Croute F, Fink GR. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 1984;197:345-6
7. Brown CA, Murray AW, Verstrepen KJ. Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 2010;20:895-903
8. Carlson M, Botstein D. Two differentially regulated mRNAs with different 5' ends encode secreted and intracellular forms of yeast invertase. Cell 1982;28:145-54
9. Carlson M, Botstein D. Organization of the SUC gene family in Saccharomyces. Mol Cell Biol 1983;3:351-9
10. CarlsonM, Osmond BC, Botstein D.Mutants of yeast defective in sucrose utilization. Genetics 1981;98:25-40
11. De Kok S, Nijkamp JF, Oud B et al. Laboratory evolution of new lactate transporter genes in a jen1Δ mutant of Saccharomyces cerevisiae and their identification as ADY2 alleles by whole-genome resequencing and transcriptome analysis. FEMS Yeast Res 2012;12:359-74
12. de Kok S, Yilmaz D, Suir E et al. Increasing free-energy (ATP) conservation in maltose-grown Saccharomyces cerevisiae by expression of a heterologous maltose phosphorylase. Metab Eng 2011;13:518-26
13. Della-Bianca BE, Basso TO, Stambuk BU et al. What do we know about the yeast strains from the Brazilian fuel ethanol industry? Appl Microbiol Biot 2013;97:979-91
14. Della-Bianca BE, de Hulster E, Pronk JT et al. Physiology of the fuel ethanol strain Saccharomyces cerevisiae PE-2 at low pH indicates a context-dependent performance relevant for industrial applications. FEMS Yeast Res 2014;14:1196-205
15. Deng X, Petitjean M, Teste M-A et al. Similarities and differences in the biochemical and enzymological properties of the four isomaltases from Saccharomyces cerevisiae. FEBS Open Bio 2014;4:200-12
16. DiCarlo JE, Norville JE, Mali P et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res 2013;41:4336-43
17. Entian KD, Kötter P. 25 yeast genetic strain and plasmid collections. Methods Microbiol 2007;36:629-66
18. Gibson AW, Wojciechowicz LA, Danzi SE et al. Constitutive mutations of the Saccharomyces cerevisiae mal-activator genes MAL23, MAL43, MAL63, and MAL64. Genetics 1997;146: 1287-98
19. Gietz BRD, Woods RA. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 2002;350:87-96
20. Gombert AK, van Maris AJ. Improving conversion yield of fermentable sugars into fuel ethanol in 1st generation yeastbased production processes. Curr Opin Biotechnol 2015;33: 81-6
21. Gueldener U, Heinisch J, Koehler GJ et al. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 2002;30:e23
22. Hawthorne DC. The genetics of alpha-methyl-glucoside fermentation in saccharomyces. Heredity (Edinb) 1958;12:273-84
23. Horák J. Regulations of sugar transporters: insights from yeast. Curr Genet 2013;59:1-31
24. Hu Z, Nehlin JO, Ronne H et al. MIG1-dependent and MIG1-independent glucose regulation of MAL gene expression in Saccharomyces cerevisiae. Curr Genet 1995;28:258-66
25. Hughes TR, Roberts CJ, Dai H et al. Widespread aneuploidy revealed by DNA microarray expression profiling. Nat Genet 2000;25:333-7
26. Krieble VK. Activities and the hydrolysis of sucrose with concentrated acids. J Am Chem Soc 1935;57:15-9
27. Kuijpers NG, Solis-Escalante D, Bosman L et al. A versatile, efficient strategy for assembly of multi-fragment expression vectors in Saccharomyces cerevisiae using 60 bp synthetic recombination sequences. Microb Cell Fact 2013;12:47
28. Lagunas R. Sugar transport in Saccharomyces cerevisiae. FEMS Microbiol Rev 1993;10:229-42
29. Liu G, Yong MYJ, Yurieva M et al. Gene essentiality is a quantitative property linked to cellular evolvability. Cell 2015;163:1388-99
30. Lowry OH, Rosebrough NJ, Farr AL et al. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75
31. Maiorella BL, Blanch HW, Wilke CR. Economic evaluation of alternative ethanol fermentation processes. Biotechnol Bioeng 1984;26:1003-25
32. Mans R, van RossumHM, WijsmanMet al. CRISPR/Cas9: amolecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res 2015;15, DOI: 10.1093/femsyr/fov004
33. Marques WL, Raghavendran V, Stambuk BU et al. Sucrose and Saccharomyces cerevisiae: a relationship most sweet. FEMS Yeast Res 2016:16, DOI: 10.1093/femsyr/fov107
34. Meadows AL, Hawkins KM, Tsegaye Y et al. Rewriting yeast central carbon metabolism for industrial isoprenoid production. Nature 2016;537:694-7
35. Mieczkowski PA, Lemoine FJ, Petes TD. Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 2006;5:1010-20
36. Mitchell DA. Note on Rising Food Prices. The World Bank Development Prospects Group, 2008. http://www.bio-based.eu/foodcrops/media/08-07ANoteonRisingFoodPrices.pdf (date last accessed, 10 August 2016)
37. Mumberg D, Müller R, Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995;156:119-22
38. Naumoff DG. Hierarchical classification of glycoside hydrolases. Biochemistry 2011;76:622-35
39. Naumoff DG, Naumov GI. Discovery of a novel family of a-glucosidase IMA genes in yeast Saccharomyces cerevisiae. Dokl Biochem Biophys 2010;432:549-51
40. 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
41. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002;30:e36
42. Piper MDW, Daran-Lapujade P, Bro C et al. Reproducibility of oligonucleotide microarray transcriptome analyses. An interlaboratory comparison using chemostat cultures of Saccharomyces cerevisiae. J Biol Chem 2002;277:37001-8
43. Postma E, Verduyn C, Scheffers WA. et al. Enzymic analysis of the crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl Environ Microb 1989;55:468-77
44. Pougach K, Voet A, Kondrashov FA et al. Duplication of a promiscuous transcription factor drives the emergence of a newregulatory network. Nat Commun 2014;5:4868
45. Ran F, Bali M, Michels CA. Hsp90/Hsp70 chaperone machine regulation of the saccharomyces MAL-activator as determined in vivo using noninducible and constitutive mutant alleles. Genetics 2008;179:331-43
46. SchmittME, Brown T, Trumpower BL. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 1990;18:3091-2
47. Sirenko OI, Ni B, Needleman RB. Purification and binding properties of theMal63p activator of Saccharomyces cerevisiae. Curr Genet 1995;27:509-16
48. 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
49. Stambuk BU, da SilvaMA, Panek AD et al. Active alpha-glucoside transport in Saccharomyces cerevisiae. FEMS Microbiol Lett 1999;170:105-10
50. Teste M-A, Duquenne M, François JM et al. Validation of reference genes for quantitative expression analysis by realtime RT-PCR in Saccharomyces cerevisiae. BMC Mol Biol 2009; 10:99
51. Teste M-A, François JM, Parrou J-L. Characterization of a new multigene family encoding isomaltases in the yeast Saccharomyces cerevisiae, the IMA family. J Biol Chem 2010;285: 26815-24
52. Van den Broek M, Bolat I, Nijkamp JF et al. Chromosomal copy number variation in Saccharomyces pastorianus is evidence for extensive genome dynamics in industrial lager brewing strains. Appl Environ Microb 2015;81:6253-67
53. Verduyn C, Postma E, ScheffersWA 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
54. Voordeckers K, Brown CA, Vanneste K et al. Reconstruction of ancestral metabolic enzymes revealsmolecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biol 2012;10:e1001446
55. Weinhandl K, Winkler M, Glieder A et al. Carbon source dependent promoters in yeasts. Microb Cell Fact 2014;13:5
56. Winge O, Roberts C. The relation between the polymeric genes for maltose raffinose, and sucrose fermentation in yeasts. Cr Trav Lab Carlsb 1952;25:141-71
57. Winzeler EA, Shoemaker DD, Astromoff A et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999;285:901-906
58. Wolfenden R, Yuan Y. Rates of spontaneous cleavage of glucose, fructose, sucrose, and trehalose in water, and the catalytic proficiencies of invertase and trehalase. J Am Chem Soc 2008;130:7548-9
59. Yamamoto K, Nakayama A, Yamamoto Y et al. Val216 decides the substrate specificity of alpha-glucosidase in Saccharomyces cerevisiae. Eur J Biochem 2004;271:3414-20
60. Zelle RM, Trueheart J, Harrison JC et al. Phosphoenolpyruvate carboxykinase as the sole anaplerotic enzyme in Saccharomyces cerevisiae. Appl Environ Microb 2010;76:5383-9
61. Zhou Y, Grof CP, Patrick JW. Proof of concept for a novel functional screening system for plant sucrose effluxers. J Biol Methods 2014;1:1-6