Engineering of Saccharomyces cerevisiae for the production of dihydroxyacetone (DHA) from sugars: A proof of concept

Metabolic Engineering

Volumn 11, Issue 6, 2009, Pages 335-346

  Nguyen, H T T ^a,b,c   Nevoigt, E ^a,b,c  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Dihydroxyacetone; Glycerol dehydrogenase; Metabolic engineering; Saccharomyces cerevisiae; Yeast

Indexed keywords

DELETION MUTANTS; DIFFERENT MICROBIAL SOURCES; DIHYDROXYACETONE; DIHYDROXYACETONE PHOSPHATE; GLYCEROL DEHYDROGENASE; GLYCEROL PRODUCTION; HANSENULA POLYMORPHA; KINASE ACTIVITY; METABOLIC ENGINEERING; OSMOTIC STRESS; OXIDIZING ACTIVITY; PROOF OF CONCEPT; S.CEREVISIAE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE YEAST; SHAKE-FLASK EXPERIMENTS; WILD-TYPE LEVELS; YEAST SACCHAROMYCES CEREVISIAE;

ENZYMES; GLUCOSE; GLYCEROL; INDUSTRIAL APPLICATIONS; METABOLISM; SUGAR (SUCROSE);

YEAST;

DIHYDROXYACETONE; GLYCEROL; GLYCEROL DEHYDROGENASE;

ARTICLE; CONTROLLED STUDY; DRUG SYNTHESIS; ENZYME ACTIVITY; ESCHERICHIA COLI; FERMENTATION; GENE EXPRESSION; METABOLIC ENGINEERING; NONHUMAN; OSMOTIC STRESS; PICHIA ANGUSTA; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

CARBOHYDRATE METABOLISM; DIHYDROXYACETONE; FEASIBILITY STUDIES; GENETIC ENHANCEMENT; GLYCEROL; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SUGAR ALCOHOL DEHYDROGENASES;

PICHIA ANGUSTA; SACCHAROMYCES CEREVISIAE;

EID: 70449727651     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2009.07.005     Document Type: Article

References (88)

1. Akin F.J., and Marlowe E. Non-carcinogenicity of dihydroxyacetone by skin painting. J. Environ. Pathol. Toxicol. Oncol. 5 (1984) 349-351
2. Albertyn J., Hohmann S., and Prior B.A. Characterization of the osmotic-stress response in Saccharomyces cerevisiae: osmotic stress and glucose repression regulate glycerol-3-phosphate dehydrogenase independently. Curr. Genet. 25 (1994) 12-18
3. Albertyn J., Hohmann S., Thevelein J.M., and Prior B.A. GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol. Cell. Biol. 14 (1994) 4135-4144
4. Ameyama M., Shinagawa E., Matsushita K., and Adachi O. Solubilization, purification and properties of membrane-bound glycerol dehydrogenase from Gluconobacter industrius. Agric. Biol. Chem. 49 (1985) 1001-1010
5. Asnis R., and Brodie A. A glycerol dehydrogenase from Escherichia coli. J. Biochem. 203 (1953) 153-159
6. Bakker B.M., Overkamp K.M., van Maris A.J., Kotter P., Luttik M.A., van Dijken J.P., and Pronk J.T. Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 25 (2001) 15-37
7. Bauer R., Katsikis N., Varga S., and Hekmat D. Study of the inhibitory effect of the product dihydroxyacetone on Gluconobacter oxydans in a semi-continuous two-stage repeated-fed-batch process. Bioprocess Biosyst. Eng. 28 (2005) 37-43
8. Bergmeyer H.U. Methods of Enzymatic Analysis vol. 3 (1974), Verlag Chemie, Weinheim (pp. 566-570)
9. Bitter G.A., and Egan K.M. Expression of heterologous genes in Saccharomyces cerevisiae from vectors utilizing the glyceraldehyde-3-phosphate dehydrogenase gene promoter. Gene 32 (1984) 263-274
10. Blomberg A. Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: questions, some answers and a model. FEMS Microbiol. Lett. 182 (2000) 1-8
11. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
12. Castells J., Geijo F., and Calahorra F. The "Formoin Reaction": a promising entry to carbohydrates from formaldehyde. Tetrahedron Lett. 27 (1980) 4517-4520
13. Charmantray F., El Blidi L., Gefflaut T., Hecquet L., Bolte J., and Lemaire M. Improved straightforward chemical synthesis of dihydroxyacetone phosphate through enzymatic desymmetrization of 2,2-dimethoxypropane-1,3-diol. J. Org. Chem. 69 (2004) 9310-9312
14. Cimprich P., Slavik J., and Kotyk A. Distribution of individual cytoplasmic pH values in a population of the yeast Saccharomyces cerevisiae. FEMS Microbiol. Lett. 130 (1995) 245-251
15. Claret C., Bories A., and Soucaille P. Glycerol inhibition of growth and dihydroxyacetone production by Gluconobacter oxydans. Curr. Microbiol. 25 (1992) 149-155
16. Cordier H., Mendes F., Vasconcelos I., and Francois J.M. A metabolic and genomic study of engineered Saccharomyces cerevisiae strains for high glycerol production. Metab. Eng. 9 (2007) 364-378
17. Córdova A., Notz W., and Barbas C.F. Direct organocatalytic aldol reactions in buffered aqueous media. Chem. Commun. (2002) 3024-3025
18. Costenoble R., Valadi H., Gustafsson L., Niklasson C., and Franzen C.J. Microaerobic glycerol formation in Saccharomyces cerevisiae. Yeast 16 (2000) 1483-1495
19. de Koning W., Weusthuis R., Harder W., and Dijkhuizen L. Methanol-dependent production of dihydroxyacetone and glycerol by mutants of the methylotrophic yeast Hansenula polymorpha blocked in dihydroxyacetone kinase and glycerol kinase. Appl. Microbiol. Biotechnol. 32 (1990) 693-698
20. Deppenmeier U., Hoffmeister M., and Prust C. Biochemistry and biotechnological applications of Gluconobacter strains. Appl. Microbiol. Biotechnol. 60 (2002) 233-242
21. Enders D., Voith M., and Lenzen A. The dihydroxyacetone unit-a versatile C(3) building block in organic synthesis. Angew. Chem. Int. Ed. Engl. 44 (2005) 1304-1325
22. Faurschou A., and Wulf H.C. Durability of the sun protection factor provided by dihydroxyacetone. Photodermatol. Photoimmunol. Photomed. 20 (2004) 239-242
23. Ferreira C., van Voorst F., Martins A., Neves L., Oliveira R., Kielland-Brandt M.C., Lucas C., and Brandt A. A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol. Biol. Cell 16 (2005) 2068-2076
24. Funk M., Niedenthal R., Mumberg D., Brinkmann K., Ronicke V., and Henkel T. Vector systems for heterologous expression of proteins in Saccharomyces cerevisiae. Methods Enzymol. 350 (2002) 248-257
25. Gancedo J.M. Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 62 (1998) 334-361
26. Gatgens C., Degner U., Bringer-Meyer S., and Herrmann U. Biotransformation of glycerol to dihydroxyacetone by recombinant Gluconobacter oxydans DSM 2343. Appl. Microbiol. Biotechnol. 76 (2007) 553-559
27. Geertman J.M., van Maris A.J., van Dijken J.P., and Pronk J.T. Physiological and genetic engineering of cytosolic redox metabolism in Saccharomyces cerevisiae for improved glycerol production. Metab. Eng. 8 (2006) 532-542
28. Gonzalez R., Murarka A., Dharmadi Y., and Yazdani S.S. A new model for the anaerobic fermentation of glycerol in enteric bacteria: trunk and auxiliary pathways in Escherichia coli. Metab Eng. 10 (2008) 234-245
29. Gueldener U., Heinisch J., Koehler G.J., Voss D., and Hegemann J.H. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30 (2002) e23
30. Hoffman C.S., and Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of E. coli. Gene 57 (1987) 267-272
31. Holst O., Lundbäck H., and Mattiasson B. Hydrogen peroxide as an oxygen source for immobilized Gluconobacter oxydans converting glycerol to dihydroxyacetone. Appl. Microbiol. Biotechnol. 22 (1985) 383-388
32. Hur E., and Wilson D.K. The crystal structure of the GCY1 protein from S. cerevisiae suggests a divergent aldo-keto reductase catalytic mechanism. Chem. Biol. Interact. 130-132 (2001) 527-536
33. Ivy J.L. Effect of pyruvate and dihydroxyacetone on metabolism and aerobic endurance capacity. Med. Sci. Sports Exerc. 30 (1998) 837-843
34. Izawa S., Sato M., Yokoigawa K., and Inoue Y. Intracellular glycerol influences resistance to freeze stress in Saccharomyces cerevisiae: analysis of a quadruple mutant in glycerol dehydrogenase genes and glycerol-enriched cells. Appl. Microbiol. Biotechnol. 66 (2004) 108-114
35. Izuo N., Nabe K., Yamada S., and Chibata I. Production of dihydroxyacetone by continuous cultivation of Acetobacter suboxydans. J. Ferment. Technol. 58 (1980) 221-226
36. Johnson E.A., and Lin E.C. Klebsiella pneumoniae 1,3-propanediol:NAD+ oxidoreductase. J. Bacteriol. 169 (1987) 2050-2054
37. Kato H., Shimao H., and Sakazawa C. Dihydroxyacetone production from methanol by a dihydroxyacetone kinase deficient mutant of Hansenula polymorpha. Appl. Microbol. Biotechnol. 23 (1986)
38. Koeller K.M., and Wong C.H. Emerging themes in medicinal glycoscience. Nat. Biotechnol. 18 (2000) 835-841
39. Klein C.J., Olsson L., and Nielsen J. Glucose control in Saccharomyces cerevisiae: the role of Mig1 in metabolic functions. Microbiology. 144 (1998) 13-24
40. Lee W., and Dasilva N.A. Application of sequential integration for metabolic engineering of 1,2-propanediol production in yeast. Metab. Eng. 8 (2006) 58-65
41. Liepins J., Kuorelahti S., Penttila M., and Richard P. Enzymes for the NADPH-dependent reduction of dihydroxyacetone and d-glyceraldehyde and l-glyceraldehyde in the mould Hypocrea jecorina. FEBS J. 273 (2006) 4229-4235
42. Liu Z., Hu Z., Zheng Y., and Shen Y. Optimization of cultivation conditions for the production of 1,3-dihydroxyacetone by Pichia membranifaciens using response surface methodology. J. Biochem. Eng. 38 (2008) 285-291
43. Mishra R., Jain S.R., and Kumar A. Microbial production of dihydroxyacetone. Biotechnol. Adv. 26 (2008) 293-303
44. Molin M., Norbeck J., and Blomberg A. Dihydroxyacetone kinases in Saccharomyces cerevisiae are involved in detoxification of dihydroxyacetone. J. Biol. Chem. 278 (2003) 1415-1423
45. Musti A.M., Zehner Z., Bostian K.A., Paterson B.M., and Kramer R.A. Transcriptional mapping of two yeast genes coding for glyceraldehyde 3-phosphate dehydrogenase isolated by sequence homology with the chicken gene. Gene 25 (1983) 133-143
46. Nabe K., Izuo N., Yamada S., and Chibata I. Conversion of glycerol to dihydroxyacetone by immobilized whole cells of Acetobacter xylinum. Appl. Environ. Microbiol. 38 (1979) 1056-1060
47. Neijssel O.M., Hueting S., Crabbendam K.J., and Tempest D.W. Dual pathways of glycerol assimilation in Klebsiella aerogenes NCIB418: their regulation and possible functional significance. Arch. Microbiol. 104 (1975) 83-87
48. Nevoigt E. Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 72 (2008) 379-412
49. Nevoigt E., and Stahl U. Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 21 (1997) 231-241
50. Niknahad H., and O'Brien P.J. Antidotal effect of dihydroxyacetone against cyanide toxicity in vivo. Toxicol. Appl. Pharmacol. 138 (1996) 186-191
51. Norbeck J., and Blomberg A. Metabolic and regulatory changes associated with growth of Saccharomyces cerevisiae in 1.4 M NaCl. Evidence for osmotic induction of glycerol dissimilation via the dihydroxyacetone pathway. J. Biol. Chem. 272 (1997) 5544-5554
52. Norbeck J., and Blomberg A. The level of cAMP-dependent protein kinase A activity strongly affects osmotolerance and osmo-instigated gene expression changes in Saccharomyces cerevisiae. Yeast 16 (2000) 121-137
53. Nordström K. Yeast growth and glycerol formation. Acta Chem. Scand. 20 (1966) 1016-1025
54. Ohrem H., and Voss H. Inhibitory effects of dihydroxyacetone on Gluconobacter cultures. Biotechnol. Lett. 17 (1995) 981-984
55. Oliveira R., Lages F., Silva-Graca M., and Lucas C. Fps1p channel is the mediator of the major part of glycerol passive diffusion in Saccharomyces cerevisiae: artefacts and re-definitions. Biochim. Biophys. Acta 1613 (2003) 57-71
56. Overkamp K.M., Bakker B.M., Kotter P., Luttik M.A., Van Dijken J.P., and Pronk J.T. Metabolic engineering of glycerol production in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 68 (2002) 2814-2821
57. Petersen A.B., Na R., and Wulf H.C. Sunless skin tanning with dihydroxyacetone delays broad-spectrum ultraviolet photocarcinogenesis in hairless mice. Mutat. Res. 542 (2003) 129-138
58. Prior B.A., and Hohmann S. Glycerol Production and Osmoregulation (1997), Technomic Publishing Company, Inc., Lancaster, PA, USA
59. Ramasastry S.S., Albertshofer K., Utsumi N., and Iii C.F. Water-compatible organocatalysts for direct asymmetric syn-aldol reactions of dihydroxyacetone and aldehydes. Org. Lett. 10 (2008) 1621-1624
60. Ramasastry S.S., Albertshofer K., Utsumi N., Tanaka F., and Barbas C.F. Mimicking fructose and rhamnulose aldolases: organocatalytic syn-aldol reactions with unprotected dihydroxyacetone. Angew. Chem. Int. Ed. Engl. 46 (2007) 5572-5575
61. Ro Y.T., Eom C.Y., Song T., Cho J.W., and Kim Y.M. Dihydroxyacetone synthase from a methanol-utilizing carboxydobacterium, Acinetobacter sp. strain JC1 DSM 3803. J. Bacteriol. 179 (1997) 6041-6047
62. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. second ed (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
63. Sharp P.M., Cowe E., Higgins D.G., Shields D.C., Wolfe K.H., and Wright F. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. Nucleic Acids Res. 16 (1988) 8207-8211
64. Sherman F., Fink G.R., and Hicks J.B. Methods in Yeast Genetics: A Laboratory Manual (1986), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
65. St. Martin E.J., Freedberg W.B., and Lin E.C.C. Kinase replacement by a dehydrogenase for Escherichia coli glycerol utilization. J. Bacteriol. 131 (1977) 1026-1028
66. Stanko R.T., Robertson R.J., Galbreath R.W., Reilly J.J., Greenawalt K.D., and Goss F.L. Enhanced leg exercise endurance with a high-carbohydrate diet and dihydroxyacetone and pyruvate. J. Appl. Physiol. 69 (1990) 1651-1656
67. Stephanopoulos G. Challenges in engineering microbes for biofuels production. Science 315 (2007) 801-804
68. Subedi K.P., Kim I., Kim J., Min B., and Park C. Role of GldA in dihydroxyacetone and methylglyoxal metabolism of Escherichia coli K12. FEMS Microbiol. Lett. 279 (2008) 180-187
69. Suga Y., Ikejima A., Matsuba S., and Ogawa H. Medical pearl: DHA application for camouflaging segmental vitiligo and piebald lesions. J. Am. Acad. Dermatol. 47 (2002) 436-438
70. Suri J.T., Mitsumori S., Albertshofer K., Tanaka F., and Barbas C.F. Dihydroxyacetone variants in the organocatalytic construction of carbohydrates: mimicking tagatose and fuculose aldolases. J. Org. Chem. 71 (2006) 3822-3828
71. Svitel J., and Sturdik E. Product yield and by-product formation in gylcerol conversion to dihydroxyacetone by Gluconobacter oxydans. J. Ferment. Technol. 78 (1994) 351-355
72. Takayama S., McGarvey G.J., and Wong C.H. Microbial aldolases and transketolases: new biocatalytic approaches to simple and complex sugars. Annu. Rev. Microbiol. 51 (1997) 285-310
73. Tamas M.J., Karlgren S., Bill R.M., Hedfalk K., Allegri L., Ferreira M., Thevelein J.M., Rydstrom J., Mullins J.G., and Hohmann S. A short regulatory domain restricts glycerol transport through yeast Fps1p. J. Biol. Chem. 278 (2003) 6337-6345
74. Tamas M.J., Luyten K., Sutherland F.C., Hernandez A., Albertyn J., Valadi H., Li H., Prior B.A., Kilian S.G., Ramos J., Gustafsson L., Thevelein J.M., and Hohmann S. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol. Microbiol. 31 (1999) 1087-1104
75. Tang C.T., Ruch F.E., and Lin C.C. Purification and properties of a nicotinamide adenine dinucleotide-linked dehydrogenase that serves an Escherichia coli mutant for glycerol catabolism. J. Bacteriol. 140 (1979) 182-187
76. Tani Y., and Yamada K. Diversity in glycerol metabolism of methylotrophic yeasts. FEMS Microbiol. Lett. 40 (1987) 151-153
77. Tani Y., and Yamada K. Glycerol metabolism in methylotrophic yeasts. Agric. Biol. Chem. 51 (1987) 1927-1933
78. Thomas B.J., and Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell. 56 (1989) 619-630
79. Thorsen M., Di Y., Tangemo C., Morillas M., Ahmadpour D., Van der Does C., Wagner A., Johansson E., Boman J., Posas F., Wysocki R., and Tamas M.J. The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol. Biol. Cell 17 (2006) 4400-4410
80. Tkac J., Navratil M., Sturdik E., and Gemeiner P. Monitoring of dihydroxyacetone production during oxidation of glycerol by immobilized Gluconobacter oxydans cells with an enzyme biosensor. Enzyme Microb. Technol. 28 (2001) 383-388
81. Truniger V., and Boos W. Mapping and cloning of gldA, the structural gene of the Escherichia coli glycerol dehydrogenase. J. Bacteriol. 176 (1994) 1796-1800
82. Utsumi N., Imai M., Tanaka F., Ramasastry S.S., and Barbas C.F. Mimicking aldolases through organocatalysis: syn-selective aldol reactions with protected dihydroxyacetone. Org. Lett. 9 (2007) 3445-3448
83. Verduyn C., Postma E., Scheffers W.A., and Van Dijken J.P. Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8 (1992) 501-517
84. Wei, S., Song, Q., Wei, D., 2007. Repeated use of immobilized Gluconobacter oxydans cells for conversion of glycerol to dihydroxyacetone. Prep. Biochem. Biotechnol. 37, 67-76.
85. Wethmar M., and Deckwer W.D. Semisynthetic culture medium for growth and dihydroxyacetone production by Gluconobacter oxydans. Biotechnol. Tech. 13 (1999) 283-287
86. Wittgenstein E., and Berry H.K. Staining of skin with dihydroxyacetone. Science 13 (1960) 894-895
87. Yamada-Onodera, K., Yamamoto, H., Emoto, E., Kawahara, N., Tani, Y., 2002. Charaterisation of glycerol dehydrogenase from a methylotrophic yeast Hansenula polymorpha DL-1, and its gene cloning. Acta. Biotechnol. 22, 337-353 〈http://cat.inist.fr/?aModele=afficheN&cpsidt=13787819〉
88. Yazdani S.S., and Gonzalez R. Anaerobic fermentation of glycerol: a path to economic viability for the biofuels industry. Curr. Opin. Biotechnol. 18 (2007) 213-219