Engineering of hydroxymandelate synthases and the aromatic amino acid pathway enables de novo biosynthesis of mandelic and 4-hydroxymandelic acid with Saccharomyces cerevisiae

Metabolic Engineering

Volumn 45, Issue , 2018, Pages 246-254

  Reifenrath, Mara ^a   Boles, Eckhard ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

4 hydroxymandelic acid; Aromatic amino acid pathway engineering; Hydroxymandelate synthase; Mandelic acid; Protein engineering; Saccharomyces cerevisiae

Indexed keywords

AMINO ACIDS; AROMATIC COMPOUNDS; AROMATIZATION; BIOCHEMISTRY; ENZYMES; YEAST;

AROMATIC AMINO ACID; MANDELIC ACID; MICROBIAL FERMENTATION; PROTEIN ENGINEERING; SUBSTRATE-BINDING SITES; SUSTAINABLE PRODUCTION; SYNTHASES; YEAST SACCHAROMYCES CEREVISIAE;

SUBSTRATES;

4 HYDROXYMANDELIC ACID; 4 HYDROXYPHENYLPYRUVATE; AROMATIC AMINO ACID; BACTERIAL ENZYME; GLUCOSE; HYDROXYMANDELATE SYNTHASE; MANDELIC ACID DERIVATIVE; PHENYLPYRUVIC ACID; SHIKIMIC ACID; SYNTHETASE; TRYPTOPHAN; UNCLASSIFIED DRUG; 4-HYDROXYMANDELIC ACID; BACTERIAL PROTEIN; DIOXYGENASE; MANDELIC ACID;

AMYCOLATOPSIS; AMYCOLATOPSIS ORIENTALIS; ARTICLE; BINDING SITE; BIOSYNTHESIS; BIOTECHNOLOGICAL PRODUCTION; CELL DENSITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; FERMENTATION; FUNGAL CELL; FUNGAL GENOME; FUNGAL STRAIN; FUNGUS GROWTH; GENE EXPRESSION; HYDROGEN BOND; NOCARDIA; NOCARDIA UNIFORMIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; SACCHAROMYCES CEREVISIAE; TRANSAMINATION; ACTINOBACTERIA; ENZYMOLOGY; GENETICS; METABOLISM;

ACTINOBACTERIA; AMINO ACIDS, AROMATIC; BACTERIAL PROTEINS; DIOXYGENASES; MANDELIC ACIDS; SACCHAROMYCES CEREVISIAE;

EID: 85041360538     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2018.01.001     Document Type: Article

References (45)

1. Adeboye, P.T., Bettiga, M., Olsson, L., The chemical nature of phenolic compounds determines their toxicity and induces distinct physiological responses in Saccharomyces cerevisiae in lignocellulose hydrolysates. AMB Express, 4, 2014, 46, 10.1186/s13568-014-0046-7.
2. Bhushan, R., Agarwal, C., Direct enantiomeric TLC resolution of dl- penicillamine using (R)-mandelic acid and l-tartaric acid as chiral impregnating reagents and as chiral mobile phase additive. Biomed. Chromatogr. 22 (2008), 1237–1242, 10.1002/bmc.
3. Braus, G.H., Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae: a model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol. Rev. 55 (1991), 349–370.
4. Brownlee, J., He, P., Moran, G.R., Harrison, D.H.T., Two roads diverged: the structure of hydroxymandelate synthase from Amycolatopsis orientalis in complex with 4-hydroxymandelate. Biochemistry 47 (2008), 2002–2013, 10.1021/bi701438r.
5. Bruder, S., Reifenrath, M., Thomik, T., Boles, E., Herzog, K., Parallelised online biomass monitoring in shake flasks enables efficient strain and carbon source dependent growth characterisation of Saccharomyces cerevisiae. Microb. Cell Fact., 15, 2016, 127, 10.1186/s12934-016-0526-3.
6. Chang, T.L., Teleshova, N., Rapista, A., Paluch, M., Anderson, R.A., Waller, D.P., Zaneveld, L.J.D., Granelli-Piperno, A., Klotman, M.E., SAMMA, a mandelic acid condensation polymer, inhibits dendritic cell-mediated HIV transmission. FEBS Lett. 581 (2007), 4596–4602, 10.1016/j.febslet.2007.08.048.
7. dos Santos, L.V., Carazzolle, M.F., Nagamatsu, S.T., Sampaio, N.M.V., Almeida, L.D., Pirolla, R.A.S., Borelli, G., Corrêa, T.L.R., Argueso, J.L., Pereira, G.A.G., Unraveling the genetic basis of xylose consumption in engineered Saccharomyces cerevisiae strains. Sci. Rep., 6, 2016, 38676, 10.1038/srep38676.
8. Dower, W.J., Miller, J.F., Ragsdale, C.W., High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 16 (1988), 6127–6145, 10.1002/cbic.200700325.
9. Entian, K.D., Kötter, P., Yeast genetic strain and plasmid collections. Methods Microbiol, 2007, 10.1016/S0580-9517(06)36025-4.
10. Furlenmeier, A., Quitt, P., Vogler, K., Lanz, P., 1976. 6-Acyl derivatives of aminopenicillanic acid. US Patent 3900464.
11. Generoso, W.C., Gottardi, M., Oreb, M., Boles, E., Simplified CRISPR-Cas genome editing for Saccharomyces cerevisiae. J. Microbiol. Methods 127 (2016), 203–205, 10.1016/j.mimet.2016.06.020.
12. Gibson, B.R., Lawrence, S.J., Leclaire, J.P.R., Powell, C.D., Smart, K.A., Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol. Rev., 2007, 10.1111/j.1574-6976.2007.00076.x.
13. Gibson, D.G., Young, L., Chuang, R.-Y., Venter, J.C., Hutchison, C. a., Smith, H.O., Iii, C.A.H., America, N., Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6 (2009), 343–345, 10.1038/nmeth.1318.
14. Gietz, R.D., Schiestl, R.H., High-efficiency yeast transformation using the LiAc/SS carrier DNA / PEG method. Nat. Protoc. 2 (2008), 31–35, 10.1038/nprot.2007.13.
15. Gottardi, M., Knudsen, J.D., Prado, L., Oreb, M., Branduardi, P., Boles, E., De novo biosynthesis of trans-cinnamic acid derivatives in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 101 (2017), 4883–4893, 10.1007/s00253-017-8220-x.
16. Gottardi, M., Reifenrath, M., Boles, E., Tripp, J., Pathway engineering for the production of heterologous aromatic chemicals and their derivatives in Saccharomyces cerevisiae: bioconversion from glucose. FEMS Yeast Res. 17 (2017), 1–22, 10.1093/femsyr/fox035.
17. Grote, A., Hiller, K., Scheer, M., Münch, R., Nörtemann, B., Hempel, D.C., Jahn, D., JCat: a novel tool to adapt codon usage of a target gene to its potential expression host. Nucleic Acids Res., 33, 2005, 10.1093/nar/gki376.
18. Hamacher, T., Becker, J., Gárdonyi, M., Hahn-Hägerdal, B., Boles, E., Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 148 (2002), 2783–2788, 10.1099/00221287-148-9-2783.
19. Hartmann, M., Schneider, T.R., Pfeil, A., Heinrich, G., Lipscomb, W.N., Braus, G.H., Evolution of feedback-inhibited / barrel isoenzymes by gene duplication and a single mutation. Proc. Natl. Acad. Sci. USA 100 (2003), 862–867, 10.1073/pnas.0337566100.
20. Hazelwood, L.A., Daran, J.M., Van Maris, A.J.A., Pronk, J.T., Dickinson, J.R., The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Appl. Environ. Microbiol. 74:8 (2008), 2259–2266, 10.1128/AEM.00934-08 (Erratum in Appl. Environ. Microbiol. 74, 3920).
21. Hubbard, B.K., Thomas, M.G., Walsh, C.T., Biosynthesis of L-p-hydroxyphenylglycine, a non-proteinogenic amino acid constituent of peptide antibiotics. Chem. Biol. 7 (2000), 931–942, 10.1016/S1074-5521(00)00043-0.
22. Koopman, F., Beekwilder, J., Crimi, B., van Houwelingen, A., Hall, R.D., Bosch, D., van Maris, A.J. a., Pronk, J.T., Daran, J.-M., De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae. Microb. Cell Fact., 11, 2012, 155, 10.1186/1475-2859-11-155.
23. Larsson, S., Quintana-Sáinz, A., Reimann, A., Nilvebrant, N.O., Jönsson, L.J., Influence of lignocellulose-derived aromatic compounds on oxygen-limited growth and ethanolic fermentation by Saccharomyces cerevisiae. Appl. Biochem. Biotechnol. 84–86 (2000), 617–632, 10.1385/ABAB:84-86:1-9:617.
24. Ley, J.P., Bertram, H.J., Synthesis of polyhydroxylated aromatic mandelic acid amides and their antioxidative potential. Tetrahedron 57 (2001), 1277–1282, 10.1016/S0040-4020(00)01136-4.
25. Li, F.-F., Zhao, Y., Li, B.-Z., Qiao, J.-J., Zhao, G.-R., Engineering Escherichia coli for production of 4-hydroxymandelic acid using glucose–xylose mixture. Microb. Cell Fact., 15, 2016, 90, 10.1186/s12934-016-0489-4.
26. Li, M., Kildegaard, K.R., Chen, Y., Rodriguez, A., Borodina, I., Nielsen, J., De novo production of resveratrol from glucose or ethanol by engineered Saccharomyces cerevisiae. Metab. Eng. 32 (2015), 1–11, 10.1016/j.ymben.2015.08.007.
27. Li, M., Schneider, K., Kristensen, M., Borodina, I., Nielsen, J., Engineering yeast for high-level production of stilbenoid antioxidants. Sci. Rep., 6, 2016, 36827, 10.1038/srep36827.
28. Liu, S.P., Liu, R.X., El-Rotail, A.A.M.M., Ding, Z.Y., Gu, Z.H., Zhang, L., Shi, G.Y., Heterologous pathway for the production of l-phenylglycine from glucose by E. coli. J. Biotechnol. 186 (2014), 91–97, 10.1016/j.jbiotec.2014.06.033.
29. Liu, Z.L., Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl. Microbiol. Biotechnol. 90 (2011), 809–825, 10.1007/s00253-011-3167-9.
30. Luttik, M.A.H., Vuralhan, Z., Suir, E., Braus, G.H., Pronk, J.T., Daran, J.M., Alleviation of feedback inhibition in Saccharomyces cerevisiae aromatic amino acid biosynthesis: quantification of metabolic impact. Metab. Eng. 10 (2008), 141–153, 10.1016/j.ymben.2008.02.002.
31. McKenna, R., Thompson, B., Pugh, S., Nielsen, D.R., Rational and combinatorial approaches to engineering styrene production by Saccharomyces cerevisiae. Microb. Cell Fact., 13, 2014, 123, 10.1186/s12934-014-0123-2.
32. Müller, U., van Assema, F., Gunsior, M., Orf, S., Kremer, S., Schipper, D., Wagemans, A., Townsend, C.A., Sonke, T., Bovenberg, R., Wubbolts, M., Metabolic engineering of the E. coli L-phenylalanine pathway for the production of d-phenylglycine (d-Phg). Metab. Eng. 8 (2006), 196–208, 10.1016/j.ymben.2005.12.001.
33. Mumberg, D., Müller, R., Funk, M., Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156 (1995), 119–122, 10.1016/0378-1119(95)00037-7.
34. Nishizawa, S., Tamaki, S., Kawamura, T., Kakeya, N., Kitao, K., 1985. Mandelic acid derivatives. WO Patent 1985001046.
35. Pan, X. xia, Li, J. jing, Wang, M. gui, He, W. sen, Jia, C. sheng, Zhang, X. ming, Feng, B., Li, D. li, Zeng, Z., Oxidative decarboxylation of mandelic acid derivative by recombinant Escherichia coli: a novel method of ethyl vanillin synthesis. Biotechnol. Lett. 35 (2013), 921–927, 10.1007/s10529-013-1158-x.
36. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., Ferrin, T.E., UCSF chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004), 1605–1612, 10.1002/jcc.20084.
37. Rodriguez, A., Kildegaard, K.R., Li, M., Borodina, I., Nielsen, J., Establishment of a yeast platform strain for production of p-coumaric acid through metabolic engineering of aromatic amino acid biosynthesis. Metab. Eng. 31 (2015), 181–188, 10.1016/j.ymben.2015.08.003.
38. Romagnoli, G., Knijnenburg, T.A., Liti, G., Louis, E.J., Pronk, J.T., Daran, J.-M., Deletion of the Saccharomyces cerevisiae ARO8 gene, encoding an aromatic amino acid transaminase, enhances phenylethanol production from glucose. Yeast 32 (2015), 29–45, 10.1002/yea.
39. Romagnoli, G., Luttik, M.A.H., Kötter, P., Pronk, J.T., Daran, J.M., Substrate specificity of thiamine pyrophosphate-dependent 2-oxo-acid decarboxylases in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 78 (2012), 7538–7548, 10.1128/AEM.01675-12.
40. Sambrook, J., Fritsch, E.F., Maniatis, T., Molecular Cloning: a Laboratory Manual. 1989, Cold Spring Harb. Lab. Press, 10.1096/fj.201600781R.
41. Saravanan, P., Singh, V.K., An efficient synthesis of chiral nonracemic diamines: application in asymmetric synthesis. Tetrahedron Lett. 39 (1998), 167–170.
42. Sun, Z., Ning, Y., Liu, L., Liu, Y., Sun, B., Jiang, W., Yang, C., Yang, S., Metabolic engineering of the L-phenylalanine pathway in Escherichia coli for the production of S- or R-mandelic acid. Microb. Cell Fact., 10, 2011, 71, 10.1186/1475-2859-10-71.
43. Ward, M., Yu, B., Wyatt, V., Griffith, J., Craft, T., Neurath, A.R., Strick, N., Li, Y.Y., Wertz, D.L., Pojman, J.A., Lowe, A.B., Anti-HIV-1 activity of poly(mandelic acid) derivatives. Biomacromolecules 8 (2007), 3308–3316, 10.1021/bm070221y.
44. Weber, C., Farwick, A., Benisch, F., Brat, D., Dietz, H., Subtil, T., Boles, E., Trends and challenges in the microbial production of lignocellulosic bioalcohol fuels. Appl. Microbiol. Biotechnol. 87 (2010), 1303–1315, 10.1007/s00253-010-2707-z.
45. Whitesell, J.K., Reynolds, D., Resolution of chiral alcohols with mandelic acid. J. Org. Chem. 48 (1983), 3548–3551, 10.1021/jo00168a035.