Deletion of the Saccharomyces cerevisiae ARO8 gene, encoding an aromatic amino acid transaminase, enhances phenylethanol production from glucose

Yeast

Volumn 32, Issue 1, 2015, Pages 29-45

  Romagnoli, Gabriele ^a,b   Knijnenburg, Theo A ^c   Liti, Gianni ^d,e   Louis, Edward J ^d,f   Pronk, Jack T ^a,b,g   Daran, Jean Marc ^a,b,g  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^c INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e UNIVERSITY OF NICE SOPHIA ANTIPOLIS   (France)

^f UNIVERSITY OF LEICESTER   (United Kingdom)

^g Platform Green Synthetic Biology   (Netherlands)

Author keywords

Aromatic amino acid; Ehrlich pathway; Phenylethanol; Saccharomyces; Synthetic genetic array; Transaminase

Indexed keywords

3 DEOXY 7 PHOSPHOHEPTULONATE SYNTHASE; ALANINE; AMINOTRANSFERASE; AMMONIA; AMMONIUM SULFATE; CANAVANINE; CARBOXYLYASE; CHORISMATE MUTASE; GLUCOSE; HISTIDINE; LEUCINE; NITROGEN; PHENETHYL ALCOHOL; PHENYLACETIC ACID; PHENYLALANINE; PHENYLPYRUVIC ACID; THREONINE; TRYPTOPHAN; TYROSINE; AROMATIC AMINO ACID AMINOTRANSFERASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ALCOHOL PRODUCTION; ALLELE; ARTICLE; AUXOTROPHY; BIOTRANSFORMATION; CELL STRUCTURE; CONTROLLED STUDY; DIPLOIDY; EXCISION REPAIR; FLOW CYTOMETRY; GENE CONTROL; GENE DELETION; GENE DOSAGE; GENE IDENTIFICATION; GENE MUTATION; GENE REPRESSION; GENETIC CODE; GENETIC SCREENING; KWASHIORKOR; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; UPREGULATION; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

GENE DELETION; GLUCOSE; PHENYLETHYL ALCOHOL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSAMINASES;

EID: 84922591196     PISSN: 0749503X     EISSN: 10970061     Source Type: Journal    
DOI: 10.1002/yea.3015     Document Type: Article

References (65)

1. Alberti S, Gitler AD, Lindquist S. 2007. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24: 913-919.
2. Askree SH, Yehuda T, Smolikov S, et al. 2004. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc Natl Acad Sci U S A 101: 8658-8663.
3. Boer VM, Daran JM, Almering MJ, et al. 2005. Contribution of the Saccharomyces cerevisiae transcriptional regulator Leu3p to physiology and gene expression in nitrogen- and carbon-limited chemostat cultures. FEMS Yeast Res 5: 885-897.
4. Boer VM, Tai SL, Vuralhan Z, et al. 2007. Transcriptional responses of Saccharomyces cerevisiae to preferred and nonpreferred nitrogen sources in glucose-limited chemostat cultures. FEMS Yeast Res 7: 604-620.
5. Brachmann CB, Davies A, Cost GJ, et al. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
6. Bulfer SL, Brunzelle JS, Trievel RC. 2013. Crystal structure of Saccharomyces cerevisiae Aro8, a putative α-aminoadipate aminotransferase. Protein Sci 22: 1417-1424.
7. Canelas AB, Ras C, Pierick A, et al. 2008. Leakage-free rapid quenching technique for yeast metabolomics. Metabolomics 4: 226-239.
8. Canelas AB, Ten PA, Ras C, et al. 2009. Quantitative evaluation of intracellular metabolite extraction techniques for yeast metabolomics. Anal Chem 81: 7379-7389.
9. Chen H, Fink GR. 2006. Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20: 1150-1161.
10. Cui Z, Yang X, Shen Q, et al. 2011. Optimisation of biotransformation conditions for production of 2-phenylethanol by a Saccharomyces cerevisiae CWY132 mutant. Nat Prod Res 25: 754-759.
11. Daran-Lapujade P, Daran JM, van Maris AJ, et al. 2009. Chemostat-based micro-array analysis in baker's yeast. Adv Microb Physiol 54: 257-311.
12. de Kok S, Nijkamp JF, Oud B, et al. 2012. 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 12: 359-374.
13. Dickinson JR, Salgado LE, Hewlins MJ. 2003. The catabolism of amino acids to long chain and complex alcohols in Saccharomyces cerevisiae. J Biol Chem 278: 8028-8034.
14. Ehrlich P, Herter CA. 1904. Uber einige Verwendungen der Naphtochinonsulfosäure. Hoppe-Seyler Z Physiol Chem 41: 379-392.
15. Eikani MH, Golmohammad F, Rowshanzamir S, et al. 2005. Recovery of water-soluble constituents of rose oil using simultaneous distillation-extraction. Flavour Frag J 20: 555-558.
16. Entian KD, Kötter P. 2007. Yeast genetic strain and plasmid collections. Methods Microbiol 36: 629-666.
17. Eshkol N, Sendovski M, Bahalul M, et al. 2009. Production of 2-phenylethanol from l-phenylalanine by a stress tolerant Saccharomyces cerevisiae strain. J Appl Microbiol 106: 534-542.
18. Etschmann M, Bluemke W, Sell D, et al. 2002. Biotechnological production of 2-phenylethanol. Appl Microbiol Biotechnol 59: 1-8.
19. Etschmann MM, Sell D, Schrader J. 2005. Production of 2-phenylethanol and 2-phenylethylacetate from l-phenylalanine by coupling whole-cell biocatalysis with organophilic pervaporation. Biotechnol Bioeng 92: 624-634.
20. Fabre CE, Blanc PJ, Goma G. 1998. 2-Phenylethyl alcohol: an aroma profile. Perfum Flavor 23: 43-45.
21. Fehrmann S, Bottin-Duplus H, Leonidou A, et al. 2013. Natural sequence variants of yeast environmental sensors confer cell-to-cell expression variability. Mol Syst Biol 9. doi: 10.1038/msb.2013.53.
22. Forsberg H, Gilstring CF, Zargari A, et al. 2001. The role of the yeast plasma membrane SPS nutrient sensor in the metabolic response to extracellular amino acids. Mol Microbiol 42: 215-228.
23. Gatbonton T, Imbesi M, Nelson M, et al. 2006. Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet 2. doi: 10.1371/journal.pgen.0020035.
24. Georis I, Feller A, Tate JJ, et al. 2009. Nitrogen catabolite repression-sensitive transcription as a readout of Tor pathway regulation: the genetic background, reporter gene and GATA factor assayed determine the outcomes. Genetics 181: 861-874.
25. Giaever G, Chu AM, Ni L, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
26. Gietz RD, Woods RA. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350: 87-96.
27. Godard P, Urrestarazu A, Vissers S, et al. 2007. Effect of 21 different nitrogen sources on global gene expression in the yeast Saccharomyces cerevisiae. Mol Cell Biol 27: 3065-3086.
28. Güldener U, Heck S, Fiedler T, et al. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24: 2519-2524.
29. Hazelwood LA, Tai SL, Boer VM, et al. 2006. A new physiological role for Pdr12p in Saccharomyces cerevisiae: export of aromatic and branched-chain organic acids produced in amino acid catabolism. FEMS Yeast Res 6: 937-945.
30. Hazelwood LA, Walsh MC, Luttik MA, et al. 2009. Identity of the growth-limiting nutrient strongly affects storage carbohydrate accumulation in anaerobic chemostat cultures of Saccharomyces cerevisiae. Appl Environ Microbiol 75: 6876-6885.
31. Hazelwood LA, Daran JM, van Maris AJ, et al. 2008. The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl Environ Microbiol 74: 2259-2266.
32. wHelmstaedt K, Krappmann S, Braus GH. 2001. Allosteric regulation of catalytic activity: Escherichia coli aspartate transcarbamoylase versus yeast chorismate mutase. Microbiol Mol Biol Rev 65: 404-421.
33. Iraqui I, Vissers S, Cartiaux M, et al. 1998. Characterisation of Saccharomyces cerevisiae ARO8 and ARO9 genes encoding aromatic aminotransferases I and II reveals a new aminotransferase subfamily. Mol Gen Genet 257: 238-248.
34. Iraqui I, Vissers S, André B, et al. 1999. Transcriptional induction by aromatic amino acids in Saccharomyces cerevisiae. Mol Cell Biol 19: 3360-3371.
35. Kazemi Seresht A, Cruz AL, de Hulster E, et al. 2013. Long term adaptation of Saccharomyces cerevisiae to the burden of recombinant insulin production. Biotechnol Bioeng 110: 2749-2763.
36. Kim B, Cho BR, Hahn JS. 2014. Metabolic engineering of Saccharomyces cerevisiae for the production of 2-phenylethanol via Ehrlich pathway. Biotechnol Bioeng 111: 115-24.
37. Kitamoto K, Yoshizawa K, Ohsumi Y, et al. 1988. Dynamic aspects of vacuolar and cytosolic amino acid pools of Saccharomyces cerevisiae. J Bacteriol 170: 2683-2686.
38. Knijnenburg TA, Daran JM, van den Broek MA, et al. 2009. Combinatorial effects of environmental parameters on transcriptional regulation in Saccharomyces cerevisiae: a quantitative analysis of a compendium of chemostat-based transcriptome data. BMC Genom 10: 53-doi: 10.1186/1471-2164-10-53.
39. Knijnenburg TA, Roda O, Wan Y, et al. 2011. A regression model approach to enable cell morphology correction in high throughput flow cytometry. Mol Syst Biol 7: 531. doi: 10.1038/msb.2011.64.
40. Kradolfer P, Niederberger P, Hutter R. 1982. Tryptophan degradation in Saccharomyces cerevisiae: characterization of two aromatic aminotransferases. Arch Microbiol 133: 242-248.
41. Krappmann S, Lipscomb WN, Braus GH. 2000. Coevolution of transcriptional and allosteric regulation at the chorismate metabolic branch point of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 97: 13585-13590.
42. Kuijpers NG, Solis-Escalante D, Bosman L, et al. 2013. A versatile, efficient strategy for assembly of multi-fragment expression vectors in Saccharomyces cerevisiae using 60 bp synthetic recombination sequences. Microb Cell Fact 12: 47. doi: 10.1186/1475-2859-12-47.
43. Kunzler M, Paravicini G, Egli CM, et al. 1992. Cloning, primary structure and regulation of the ARO4 gene, encoding the tyrosine-inhibited 3-deoxy-d-arabino-heptulosonate-7-phosphate synthase from Saccharomyces cerevisiae. Gene 113: 67-74.
44. Lee K, Hahn JS. 2013. Interplay of Aro80 and GATA activators in regulation of genes for catabolism of aromatic amino acids in Saccharomyces cerevisiae. Mol Microbiol 88: 1120-1134.
45. Luttik MAH, Vuralhan Z, Suir E, et al. 2008. Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: quantification of metabolic impact. Metab Eng 10: 141-153.
46. Newman JR, Ghaemmaghami S, Ihmels J, et al. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441: 840-846.
47. Nijkamp JF, van den Broek M, Datema E, et al. 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. doi: 10.1186/1475-2859-11-36.
48. Pan X, Yuan DS, Xiang D, et al. 2004. A robust toolkit for functional profiling of the yeast genome. Mol Cell 16: 487-496.
49. Peng J, Schwartz D, Elias JE, et al. 2003. A proteomics approach to understanding protein ubiquitination. Nat Biotechnol 21: 921-926.
50. Pronk JT. 2002. Auxotrophic yeast strains in fundamental and applied research. Appl Environ Microbiol 68: 2095-2100.
51. Prusty R, Grisafi P, Fink GR. 2004. The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 101: 4153-4157.
52. Romagnoli G, Luttik MA, Kotter P, et al. 2012. Substrate specificity of thiamine pyrophosphate-dependent 2-oxo-acid decarboxylases in Saccharomyces cerevisiae. Appl Environ Microbiol 78: 7538-7548.
53. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
54. Solis-Escalante D, Kuijpers NG, Bongaerts N, et al. 2013. amdSYM, a new dominant recyclable marker cassette for Saccharomyces cerevisiae. FEMS Yeast Res 13: 126-139.
55. Stark D, Zala D, Münch T, et al. 2003. Inhibition aspects of the bioconversion of l-phenylalanine to 2-phenylethanol by Saccharomyces cerevisiae. Enzyme Microb Tech 32: 212-223.
56. Szabados L, Savouré A. 2010. Proline: a multifunctional amino acid. Trends Plant Sci 15: 89-97.
57. Tai SL, Boer VM, Daran-Lapujade P, et al. 2005. Two-dimensional transcriptome analysis in chemostat cultures. Combinatorial effects of oxygen availability and macronutrient limitation in Saccharomyces cerevisiae. J Biol Chem 280: 437-447.
58. Tong AH, Evangelista M, Parsons AB, et al. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
59. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121.
60. Urrestarazu A, Vissers S, Iraqui I, Grenson M. 1998. Phenylalanine- and tyrosine-auxotrophic mutants of Saccharomyces cerevisiae impaired in transamination. Mol Gen Genet 257: 230-237.
61. van Dam JC, Eman MR, Frank J, et al. 2002. Analysis of glycolytic intermediates in Saccharomyces cerevisiae using anion exchange chromatography and electrospray ionization with tandem mass spectrometric detection. Anal Chim Acta 460: 209-218.
62. Verduyn C, Postma E, Scheffers WA, Van Dijken JP. 1992. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous culture study on the regulation of respiration and alcoholic fermentation. Yeast 8: 501-517.
63. Vuralhan Z, Luttik MA, Tai SL, et al. 2005. Physiological characterization of the ARO10-dependent, broad-substrate-specificity 2-oxo acid decarboxylase activity of Saccharomyces cerevisiae. Appl Environ Microbiol 71: 3276-3284.
64. Vuralhan Z, Morais MA, Tai SL, et al. 2003. Identification and characterization of phenylpyruvate decarboxylase genes in Saccharomyces cerevisiae. Appl Environ Microbiol 69: 4534-4541.
65. 13C-labeled cell extracts as internal standards. Anal Biochem 336: 164-171.