Energy coupling in Saccharomyces cerevisiae: Selected opportunities for metabolic engineering

FEMS Yeast Research

Volumn 12, Issue 4, 2012, Pages 387-397

  De Kok, Stefan ^a   Kozak, Barbara U ^a   Pronk, Jack T ^a   Van Maris, Antonius J A ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

ATP; Free energy conservation; Product yield; Synthetic biology; Thermodynamics; Transport

Indexed keywords

ADENOSINE TRIPHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

CARBOXYLATION; FUNGAL METABOLISM; METABOLIC ENGINEERING; MICROBIAL DIVERSITY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RESPIRATORY CHAIN; SACCHAROMYCES CEREVISIAE; SHORT SURVEY; SUGAR TRANSPORT;

ADENOSINE TRIPHOSPHATE; ENERGY METABOLISM; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 84860258944     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2012.00799.x     Document Type: Short Survey

References (93)

1. Abbott DA, Knijnenburg TA, De Poorter LMI, Reinders MJT, Pronk JT & Van Maris AJA (2007) Generic and specific transcriptional responses to different weak organic acids in anaerobic chemostat cultures of Saccharomyces cerevisiae. FEMS Yeast Res 7: 819-833.
2. Abbott DA, Zelle RM, Pronk JT & Van Maris AJA (2009) Metabolic engineering of Saccharomyces cerevisiae for production of carboxylic acids: current status and challenges. FEMS Yeast Res 9: 1123-1136.
3. Adachi E, Torigoe M, Sugiyama M, Nikawa JI & Shimizu K (1998) Modification of metabolic pathways of Saccharomyces cerevisiae by the expression of lactate dehydrogenase and deletion of pyruvate decarboxylase genes for the lactic acid fermentation at low pH value. J Ferment Bioeng 86: 284-289.
4. Atsumi S, Hanai T & Liao JC (2008) Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451: 86-89.
5. 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.
6. Basso TO, de Kok S, Dario M et al. (2011) Engineering topology and kinetics of sucrose metabolism in Saccharomyces cerevisiae for improved ethanol yield. Metab Eng 13: 694-703.
7. Batista AS, Miletti ASBLC & Stambuk BU (2004) Sucrose fermentation by Saccharomyces cerevisiae lacking hexose transport. J Mol Microbiol Biotechnol 8: 26-33.
8. Beauprez JJ, De Mey M & Soetaert WK (2010) Microbial succinic acid production: natural versus metabolic engineered producers. Process Biochem 45: 1103-1114.
9. Becker J & Boles E (2003) A modified Saccharomyces cerevisiae strain that consumes L-arabinose and produces ethanol. Appl Environ Microbiol 69: 4144-4150.
10. Boles E & Hollenberg CP (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21: 85-111.
11. Burger M, Bacon EE & Bacon J (1961) Some observations on the form and location of invertase in the yeast cell. Biochem J 78: 504-511.
12. Canelas AB, Ras C, ten Pierick A, van Gulik WM & Heijnen JJ (2011) An in vivo data-driven framework for classification and quantification of enzyme kinetics and determination of apparent thermodynamic data. Metab Eng 13: 294-306.
13. Carlson M & Botstein D (1982) Two differentially regulated mRNAs with different 5′ ends encode secreted and intracellular forms of yeast invertase. Cell 28: 145-154.
14. Chance B & Williams G (1955) Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J Biol Chem 217: 383-393.
15. Chao YP & Liao JC (1994) Metabolic responses to substrate futile cycling in Escherichia coli. J Biol Chem 269: 5122-5126.
16. De Groeve MRM, De Baere M, Hoflack L, Desmet T, Vandamme EJ & Soetaert W (2009) Creating lactose phosphorylase enzymes by directed evolution of cellobiose phosphorylase. Protein Eng Des Sel 22: 393-399.
17. de Kok S, Yilmaz Y, Suir E, Pronk JT, Daran JM & Van Maris AJA (2011) Increasing free-energy (ATP) conservation in maltose-grown Saccharomyces cerevisiae by expression of a heterologous maltose phosphorylase. Metab Eng 13: 518-526.
18. de Vries W, van Wyck-Kapteyn W & Stouthamer A (1973) Generation of ATP during cytochrome-linked anaerobic electron transport in propionic acid bacteria. J Gen Microbiol 76: 31-41.
19. Doudoroff M (1955) Disaccharide phosphorylases. Methods Enzymol 1: 225-231.
20. Ehrmann MA & Vogel RF (1998) Maltose metabolism of Lactobacillus sanfranciscensis: cloning and heterologous expression of the key enzymes, maltose phosphorylase and phosphoglucomutase. FEMS Microbiol Lett 169: 81-86.
21. Gascón S & Lampen JO (1968) Purification of the internal invertase of yeast. J Biol Chem 243: 1567-1572.
22. + symporter in the type strain of Saccharomyces carlsbergensis. J Bacteriol 182: 5628-5630.
23. Guan L & Kaback HR (2006) Lessons from lactose permease. Annu Rev Biophys Biomol Struct 35: 67-91.
24. +-ATPase. Biochim Biophys Acta 1768: 2383-2392.
25. Henry CS, Broadbelt LJ & Hatzimanikatis V (2010) Discovery and analysis of novel metabolic pathways for the biosynthesis of industrial chemicals: 3 hydroxypropanoate. Biotechnol Bioeng 106: 462-473.
26. 2O-forming NADH oxidase and impact on redox metabolism. Metab Eng 8: 303-314.
27. Hou J, Lages NF, Oldiges M & Vemuri GN (2009) Metabolic impact of redox cofactor perturbations in Saccharomyces cerevisiae. Metab Eng 11: 253-261.
28. Huh WK & Kang SO (1999) Molecular cloning and functional expression of alternative oxidase from Candida albicans. J Bacteriol 181: 4098-4102.
29. Jamalzadeh E, Taymaz-Nikerel H, Heijnen JJ, van Gulik WM & Verheijen PJT (2012) A thermodynamic analysis of dicarboxylic acid production in microorganisms. Thermodynamics in Biochemical Engineering (von Stockar U, van der Wielen LAM & Prausnitz JM, eds). EPFL Press, Lausanne, Switzerland (In press).
30. Jansen MLA, Krook DJJ, De Graaf K, Van Dijken JP, Pronk JT & De Winde JH (2006) Physiological characterization and fed batch production of an extracellular maltase of Schizosaccharomyces pombe CBS 356. FEMS Yeast Res 6: 888-901.
31. Jantama K, Haupt M, Svoronos SA, Zhang X, Moore J, Shanmugam K & Ingram L (2008) Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate. Biotechnol Bioeng 99: 1140-1153.
32. Jiang X, Meng X & Xian M (2009) Biosynthetic pathways for 3-hydroxypropionic acid production. Appl Microbiol Biotechnol 82: 995-1003.
33. Joseph-Horne T, Hollomon DW & Wood PM (2001) Fungal respiration: a fusion of standard and alternative components. Biochim Biophys Acta 1504: 179-195.
34. Kalckar HM (1974) Origins of the concept oxidative phosphorylation. Mol Cell Biochem 5: 55-62.
35. Kerscher S, Dröse S, Zickermann V & Brandt U (2008) The three families of respiratory NADH dehydrogenases. Results Probl Cell Differ 45: 185-222.
36. Kilian SG & van Uden N (1988) Transport of xylose and glucose in the xylose-fermenting yeast Pichia stipitis. Appl Microbiol Biotechnol 27: 545-548.
37. Kim P, Laivenieks M, Vieille C & Zeikus JG (2004) Effect of overexpression of Actinobacillus succinogenes phosphoenolpyruvate carboxykinase on succinate production in Escherichia coli. Appl Environ Microbiol 70: 1238-1241.
38. Kröger A, Geisler V, Lemma E, Theis F & Lenger R (1992) Bacterial fumarate respiration. Arch Microbiol 158: 311-314.
39. Kuyper M, Toirkens MJ, Diderich JA, Winkler AA, van Dijken JP & Pronk JT (2005a) Evolutionary engineering of mixed sugar utilization by a xylose fermenting Saccharomyces cerevisiae strain. FEMS Yeast Res 5: 925-934.
40. Kuyper M, Hartog MM, Toirkens MJ, Almering MJ, Winkler AA, van Dijken JP & Pronk JT (2005b) Metabolic engineering of a xylose-isomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation. FEMS Yeast Res 5: 399-409.
41. Lagunas R (1993) Sugar transport in Saccharomyces cerevisiae. FEMS Microbiol Lett 104: 229-242.
42. Lancashire W, Dickinson J & Malloch R (1998) DNA encoding enzymes of the glycolytic pathway for use in alcohol producing yeast. US Patent Number 5786186.
43. Lee K, Skotnicki M, Tribe D & Rogers P (1980) Kinetic studies on a highly productive strain of Zymomonas mobilis. Biotechnol Lett 2: 339-344.
44. Marini AM, Soussi-Boudekou S, Vissers S & Andre B (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17: 4282-4293.
45. Millard CS, Chao YP, Liao JC & Donnelly MI (1996) Enhanced production of succinic acid by overexpression of phosphoenolpyruvate carboxylase in Escherichia coli. Appl Environ Microbiol 62: 1808-1810.
46. Nakamura CE & Whited GM (2003) Metabolic engineering for the microbial production of 1, 3-propanediol. Curr Opin Microbiol 14: 454-459.
47. Navas MA, Cerdán S & Gancedo JM (1993) Futile cycles in Saccharomyces cerevisiae strains expressing the gluconeogenic enzymes during growth on glucose. P Natl Acad Sci USA 90: 1290-1294.
48. Palmqvist E & Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74: 25-33.
49. +-ATPase. J Biol Chem 275: 15709-15716.
50. Pfromm PH, Amanor-Boadu V, Nelson R, Vadlani P & Madl R (2010) Bio-butanol vs. bio-ethanol: a technical and economic assessment for corn and switchgrass fermented by yeast or Clostridium acetobutylicum. Biomass Bioenergy 34: 515-524.
51. Piper P, Mahé Y, Thompson S, Pandjaitan R, Holyoak C, Egner R, Mühlbauer M, Coote P & Kuchler K (1998) The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J 17: 4257-4265.
52. Pronk JT, Steensma HY & Van Dijken JP (1996) Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 12: 1607-1633.
53. Raab AM & Lang C (2011) Oxidative versus reductive succinic acid production in the yeast Saccharomyces cerevisiae. Bioeng Bugs 2: 120-123.
54. Rigoulet M, Guerin B & Denis M (1987) Modification of flow force relationships by external ATP in yeast mitochondria. Eur J Biochem 168: 275-279.
55. Ro DK, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS & Kirby J (2006) Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440: 940-943.
56. Rogers P, Lee KJ & Tribe D (1979) Kinetics of alcohol production by Zymomonas mobilis at high sugar concentrations. Biotechnol Lett 1: 165-170.
57. Sadie CJ, Rose SH, den Haan R & van Zyl WH (2011) Co-expression of a cellobiose phosphorylase and lactose permease enables intracellular cellobiose utilisation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 90: 1373-1380.
58. Santos E, Rodriguez L, Elorza M & Sentandreu R (1982) Uptake of sucrose by Saccharomyces cerevisiae. Arch Biochem Biophys 216: 652-660.
59. Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 73: 129-169.
60. Sauer M, Porro D, Mattanovich D & Branduardi P (2008) Microbial production of organic acids: expanding the markets. Trends Biotechnol 26: 100-108.
61. Schlegel HG (1993) General Microbiology, 7th edn. Cambridge University Press, Cambridge, UK.
62. Serrano R (1991) Transport across yeast vacuolar and plasma membranes. The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis and Energetics (Jones EW & Broach JR, eds), 21: pp. 523-585. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
63. Sonderegger M, Schumperli M & Sauer U (2004) Metabolic engineering of a phosphoketolase pathway for pentose catabolism in Saccharomyces cerevisiae. Appl Environ Microbiol 70: 2892-2897.
64. Song H & Lee SY (2006) Production of succinic acid by bacterial fermentation. Enzyme Microb Technol 39: 352-361.
65. Sprenger GA (1996) Carbohydrate metabolism in Zymomonas mobilis: a catabolic highway with some scenic routes. FEMS Microbiol Lett 145: 301-307.
66. Stambuk BU, Batista AS & De Araujo PS (2000) Kinetics of active sucrose transport in Saccharomyces cerevisiae. J Biosci Bioeng 89: 212-214.
67. +-dependent malic enzyme in an Escherichia coli mutant. Appl Environ Microbiol 63: 2695-2701.
68. Stolz P, Böcker G, Vogel RF & Hammes WP (1993) Utilisation of maltose and glucose by lactobacilli isolated from sourdough. FEMS Microbiol Lett 109: 237-242.
69. Sutton D & Lampen J (1962) Localization of sucrose and maltose fermenting systems in Saccharomyces cerevisiae. Biochim Biophys Acta 56: 303-312.
70. Szczebara FM, Chandelier C, Villeret C, Masurel A, Bourot S, Duport C, Blanchard S, Groisillier A, Testet E & Costaglioli P (2003) Total biosynthesis of hydrocortisone from a simple carbon source in yeast. Nat Biotechnol 21: 143-149.
71. Van Gulik W & Heijnen J (1995) A metabolic network stoichiometry analysis of microbial growth and product formation. Biotechnol Bioeng 48: 681-698.
72. van Leeuwen CC, Weusthuis RA, Postma E, van den Broek PJ & van Dijken JP (1992) Maltose/proton co-transport in Saccharomyces cerevisiae. Comparative study with cells and plasma membrane vesicles. Biochem J 284: 441-445.
73. van Maris AJA, Konings WN, van Dijken JP & Pronk JT (2004a) Microbial export of lactic and 3-hydroxypropanoic acid: implications for industrial fermentation processes. Metab Eng 6: 245-255.
74. van Maris AJA, Winkler AA, Porro D, van Dijken JP & Pronk JT (2004b) Homofermentative lactate production cannot sustain anaerobic growth of engineered Saccharomyces cerevisiae: possible consequence of energy-dependent lactate export. Appl Environ Microbiol 70: 2898-2905.
75. van Maris AJA, Abbott DA, Bellissimi E, van den Brink J, Kuyper M, Luttik MAH, Wisselink HW, Scheffers WA, van Dijken JP & Pronk JT (2006) Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Antonie Van Leeuwenhoek 90: 391-418.
76. Vemuri G, Eiteman M & Altman E (2002) Effects of growth mode and pyruvate carboxylase on succinic acid production by metabolically engineered strains of Escherichia coli. Appl Environ Microbiol 68: 1715-1727.
77. Vemuri G, Eiteman M, McEwen J, Olsson L & Nielsen J (2007) Increasing NADH oxidation reduces overflow metabolism in Saccharomyces cerevisiae. P Natl Acad Sci USA 104: 2402-2407.
78. 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.
79. Vodovotz Y, Clermont G, Hunt CA, Lefering R, Bartels J, Seydel R, Hotchkiss J, Ta'asan S, Neugebauer E & An G (2007) Evidence-based modeling of critical illness: an initial consensus from the Society for Complexity in Acute Illness. J Crit Care 22: 77-84.
80. Watt IN, Montgomery MG, Runswick MJ, Leslie AGW & Walker JE (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. P Natl Acad Sci USA 107: 16823-16827.
81. Weusthuis RA, Adams H, Scheffers WA & van Dijken JP (1993) Energetics and kinetics of maltose transport in Saccharomyces cerevisiae: a continuous culture study. Appl Environ Microbiol 59: 3102-3109.
82. Weusthuis RA, Lamot I, van der Oost J & Sanders JPM (2011) Microbial production of bulk chemicals: development of anaerobic processes. Trends Biotechnol 29: 153-158.
83. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP & Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464: 123-128.
84. Wisselink HW, Toirkens MJ, Wu Q, Pronk JT & van Maris AJA (2009) Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 75: 907-914.
85. Yu C, Cao Y, Zou H & Xian M (2011) Metabolic engineering of Escherichia coli for biotechnological production of high-value organic acids and alcohols. Appl Microbiol Biotechnol 89: 1-11.
86. Zeikus J, Jain M & Elankovan P (1999) Biotechnology of succinic acid production and markets for derived industrial products. Appl Microbiol Biotechnol 51: 545-552.
87. Zelle RM, De Hulster E, Van Winden WA, De Waard P, Dijkema C, Winkler AA, Geertman JMA, Van Dijken JP, Pronk JT & van Maris AJA (2008) Malic acid production by Saccharomyces cerevisiae: engineering of pyruvate carboxylation, oxaloacetate reduction, and malate export. Appl Environ Microbiol 74: 2766-2777.
88. Zelle RM, Trueheart J, Harrison JC, Pronk JT & van Maris AJA (2010a) Phosphoenolpyruvate carboxykinase as the sole anaplerotic enzyme in Saccharomyces cerevisiae. Appl Environ Microbiol 76: 5383-5389.
89. 4-dicarboxylic acids in bioreactor batch cultures of an engineered Saccharomyces cerevisiae strain. Appl Environ Microbiol 76: 744-750.
90. Zelle RM, Harrison JC, Pronk JT & van Maris AJA (2011) Anaplerotic role for cytosolic malic enzyme in engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 77: 732-738.
91. Zhang YHP & Lynd LR (2005) Cellulose utilization by Clostridium thermocellum: bioenergetics and hydrolysis product assimilation. P Natl Acad Sci USA 102: 7321-7325.
92. Zhang X, Jantama K, Moore JC, Jarboe LR, Shanmugam KT & Ingram LO (2009) Metabolic evolution of energy-conserving pathways for succinate production in Escherichia coli. P Natl Acad Sci USA 106: 20180-20185.
93. Zhang X, Wang X, Shanmugam K & Ingram L (2011) L-Malate production by metabolically engineered Escherichia coli. Appl Environ Microbiol 77: 427-434.