Engineering NADH metabolism in Saccharomyces cerevisiae: Formate as an electron donor for glycerol production by anaerobic, glucose-limited chemostat cultures

FEMS Yeast Research

Volumn 6, Issue 8, 2006, Pages 1193-1203

  Geertman, Jan Maarten A ^a   Van Dijken, Johannes P ^a,b   Pronk, Jack T ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b Bird Engineering BV   (Netherlands)

Author keywords

Anaerobic formate metabolism; Formate dehydrogenase; Glycerol; Metabolic engineering; Mixed substrate utilization; NADH metabolism

Indexed keywords

FORMATE DEHYDROGENASE; FORMIC ACID; GLUCOSE; GLYCEROL; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; BIOENGINEERING; BIOSYNTHESIS; CHEMOSTAT; ENZYME KINETICS; FUNGAL STRAIN; FUNGUS CULTURE; NONHUMAN; OXIDATION; PROTEIN EXPRESSION; REDUCTION; SACCHAROMYCES CEREVISIAE; YEAST;

ANAEROBIOSIS; BIOREACTORS; DNA, FUNGAL; ELECTRONS; FORMIC ACIDS; GENES, FUNGAL; GLUCOSE; GLYCEROL; KINETICS; NAD; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 33751279921     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2006.00124.x     Document Type: Article

References (60)

1. Aguilera J, Petit T, de Winde JH & Pronk JT (2005) Physiological and genome-wide transcriptional responses of Saccharomyces cerevisiae to high carbon dioxide concentrations. FEMS Yeast Res 5: 579-593.
2. Albertyn J, van Tonder A & Prior BA (1992) Purification and characterization of glycerol-3-phosphate dehydrogenase of Saccharomyces cerevisiae. FEBS Lett 308: 130-132.
3. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8: 115-118.
4. +-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16: 2179-2187.
5. Arfman N, van Beeumen J, de Vries GE, Harder W & Dijkhuizen L (1991) Purification and characterization of an activator protein for methanol dehydrogenase from thermotolerant Bacillus spp. J Biol Chem 266: 3955-3960.
6. Arfman N, Hektor HJ, Bystrykh LV, Govorukhina NI, Dijkhuizen L & Frank J (1997) Properties of an NAD(H)-containing methanol dehydrogenase and its activator protein from Bacillus methanolicus. Eur J Biochem 244: 426-433.
7. Babel W, Brinkmann U & Müller RH (1993) The auxiliary substrate concept - an approach for overcoming limits of microbial performances. Acta Biotechnol 13: 211-242.
8. Bakker BM, Overkamp KM, van Maris AJA, Kötter P, Luttik MAH, van Dijken JP & Pronk JT (2001) Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol Rev 25: 15-37.
9. +-dependent formate dehydrogenase. Metab Eng 4: 217-229.
10. Blanchard JS & Cleland WW (1980) Kinetic and chemical mechanisms of yeast formate dehydrogenase. Biochemistry 19: 3543-3550.
11. +) in acquired osmotolerance of Saccharomyces cerevisiae. J Bacteriol 171: 1087-1092.
12. Bruinenberg PM, Jonker R, van Dijken JP & Scheffers WA (1985) Utilization of formate as an additional energy source by glucose-limited chemostat cultures of Candida utilis CBS 621 and Saccharomyces cerevisiae CBS 8066. Evidence for the absence of transhydrogenase activity in yeasts. Arch Microbiol 142: 302-306.
13. Casal M, Cardoso H & Leão C (1996) Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142: 1385-1390.
14. Cássio F, Leão C & van Uden N (1987) Transport of lactate and other short-chain monocarboxylates in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 53: 509-513.
15. de Jong-Gubbels P, Vanrolleghem P, Heijnen S, van Dijken JP & Pronk JT (1995) Regulation of carbon metabolism in chemostat cultures of Saccharomyces cerevisiae grown on mixtures of glucose and ethanol. Yeast 11: 407-418.
16. Egli T & Zinn M (2003) The concept of multiple-nutrient-limited growth of microorganisms and its application in biotechnological processes. Biotechnol Adv 22: 35-43.
17. Fujii T & Tonomura K (1972) Oxidation of methanol, formaldehyde and formate by a Candida species. Agric Biol Chem 36: 2297-2306.
18. Gancedo C, Gancedo JM & Sols A (1968) Glycerol metabolism in yeasts, pathways of utilization and production. Eur J Biochem 5: 165-172.
19. Gietz RD & Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 527-534.
20. Gietz RD & Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350: 87-96.
21. Gommers PJF, van Schie BJ, van Dijken JP & Kuenen JG (1988) Biochemical limits to microbial growth yields: an analysis of mixed substrate utilization. Biotechnol Bioeng 32: 86-94.
22. Hazeu W & Donker RA (1983) A continuous culture study of methanol and formate utilization by the yeast Pichia pastoris. Biotechnol Lett 5: 399-404.
23. Holzer H, Bernhardt W & Schneider S (1963) Zur Glycerinbildung in Bäckerhefe. Biochem Z 336: 495-509.
24. Inoue H, Nojima H & Okayama H (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96: 23-28.
25. Kato N, Sahm H & Wagner F (1979) Steady-state kinetics of formaldehyde dehydrogenase and formate dehydrogenase from a methanol-utilizing yeast, Candida boidinii. Biochim Biophys Acta 566: 12-20.
26. Kaup B, Bringer-Meyer S & Sahm H (2003) Metabolic engineering of Escherichia coli: construction of an efficient biocatalyst for D-mannitol formation in a whole-cell biotransformation. Commun Agric Appl Biol Sci 68: 235-240.
27. Lin S-J & Guarente L (2003) Nicotinamide adenine dinucleotide, a metabolic regulator of transcription, longevity and disease. Curr Opin Cell Biol 15: 241-246.
28. Lowry OH, Rosebrough NJ, Farr AL & Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
29. Luttik MAH, Kötter P, Salomons FA, van der Klei IJ, van Dijken JP & Pronk JT (2000) The Saccharomyces cerevisiae ICL2 gene encodes a mitochondrial 2-methylisocitrate lyase involved in propionyl-coenzyme A metabolism. J Bacteriol 182: 7007-7013.
30. Müller RH & Babel W (1996) Growth rate-dependent expression of phenol-assimilation pathways in Alcaligenes eutrophus JMP 134 - the influence of formate as an auxiliary energy source on phenol conversion characteristics. Appl Microbiol Biotechnol 46: 156-162.
31. Neuberg C & Reinfurth E (1919) Natürliche und erzwungene Glycerinbildung bei der alkoholischen Gärung. Biochem Z 92: 234-266.
32. Norbeck J, Påhlman AK, Akhtar N, Blomberg A & Adler L (1996) Purification and characterization of two isoenzymes of DL-glycerol-3-phosphatase from Saccharomyces cerevisiae. J Biol Chem 271: 13875-13881.
33. Oura (1972) The effect of aeration on the growth energetics and biochemical composition of baker's yeast. PhD Thesis. Research Laboratories of the State Alcohol Monopoly (ALKO), Helsinki.
34. Overkamp KM, Bakker BM, Kötter P, Luttik MAH, van Dijken JP & Pronk JT (2002a) Metabolic engineering of glycerol production in Saccharomyces cerevisiae. Appl Environ Microbiol 68: 2814-2821.
35. +-dependent formate dehydrogenase in Saccharomyces cerevisiae. Yeast 19: 509-520.
36. Peacock D & Boulter D (1970) Kinetic studies of formate dehydrogenase. Biochem J 120: 763-769.
37. +-dependent formate dehydrogenase. Biochem J 301: 625-643.
38. Postma E, Verduyn C, Scheffers WA & van Dijken JP (1989) Enzymic analysis of the Crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl Environ Microbiol 55: 468-477.
39. Remize F, Barnavon L & Dequin S (2001) Glycerol export and glycerol-3-phosphate dehydrogenase, but not glycerol phosphatase, are rate limiting for glycerol production in Saccharomyces cerevisiae. Metab Eng 3: 301-312.
40. Rose ZB & Racker E (1962) Formaldehyde dehydrogenase from bakers' yeast. J Biol Chem 237: 3279-3281.
41. Sambrook K, Fritsch EF & Maniatis I (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
42. Serov AE, Popova AS, Fedorchuk VV & Tishkov VI (2002) Engineering of coenzyme specificity of Saccharomyces cerevisiae formate dehydrogenase. Biochem J 367: 841-847.
43. Sies H (1982) Metabolic Compartmentation. Academic Press, London.
44. Taherzadeh MJ, Adler L & Lidén G (2002) Strategies for enhancing fermentative production of glycerol - review. Enzyme Microb Technol 31: 53-66.
45. Tai SL, Boer VM, Daran-Lapujade P, Walsh MC, de Winde JH, Daran JM & Pronk JT (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.
46. Takeshita R & Yasueda H (2004) Corynebacterium transformed to utilize methanol as carbon source. Patent No. EP1454991A1.
47. Tishkov VI & Popov VO (2004) Catalytic mechanism and application of formate dehydrogenase. Biochemistry (Moscow, Russ Fed) 69: 1252-1267.
48. Tsuboi KK & Hudson PB (1956) Acid phosphatase. VI. Kinetic properties of purified yeast and erythrocyte phosphomonoesterase. Arch Biochem Biophys 61: 197-210.
49. van den Berg MA & Steensma HY (1997) Expression cassettes for formaldehyde and fluoroacetate resistance, two dominant markers in Saccharomyces cerevisiae. Yeast 13: 551-559.
50. van Dijken JP, Harder W & Quayle JR (1981) Energy transduction and carbon assimilation in methylotrophic yeasts. Microbial growth on C1-compounds (Dalton H, ed) pp. 191-201. Heyden & Son Ltd., London, UK.
51. van Dijken JP & Scheffers WA (1986) Redox balances in the metabolism of sugars by yeast. FEMS Microbiol Rev 32: 199-224.
52. van Dijken JP, Bauer J, Brambilla L, et al. (2000) An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains. Enzyme Microb Technol 26: 706-714.
53. van Hoek P, van Dijken JP & Pronk JT (2000) Regulation of fermentative capacity and levels of glycolytic enzymes in chemostat cultures of Saccharomyces cerevisiae. Enzyme Microb Technol 26: 724-736.
54. van Maris AJA, Konings WN, van Dijken JP & Pronk JT (2004) Microbial export of lactic and 3-hydroxypropanoic acid: implications for industrial fermentation processes. Metab Eng 4: 245-255.
55. van Urk H, Mak PR, Scheffers WA & van Dijken JP (1988) Metabolic responses of Saccharomyces cerevisiae CBS 8066 and Candida utilis CBS 621 upon transition from glucose limitation to glucose excess. Yeast 4: 283-291.
56. Verduyn C (1991) Physiology of yeasts in relation to biomass yields. Antonie Van Leeuwenhoek 60: 325-353.
57. Verduyn C, Postma E, Scheffers WA & van Dijken JP (1990) Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136: 395-403.
58. 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.
59. Wandrey C (2004) Biochemical reaction engineering for redox reactions. Chem Rec 4: 254-265.
60. Zinn M, Witholt B & Egli T (2004) Dual nutrient limited growth: models, experimental observations, and applications. J Biotechnol 113: 263-279.