Engineering cytosolic acetyl-coenzyme A supply in Saccharomyces cerevisiae: Pathway stoichiometry, free-energy conservation and redox-cofactor balancing

Metabolic Engineering

Volumn 36, Issue , 2016, Pages 99-115

  van Rossum, Harmen M ^a   Kozak, Barbara U ^a   Pronk, Jack T ^a   van Maris, Antonius J A ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Acetylating acetaldehyde dehydrogenase; ATP citrate lyase; Carnitine shuttle; Phosphoketolase; Pyruvate dehydrogenase; Pyruvate formate lyase

Indexed keywords

CELL ENGINEERING; COENZYMES; ENERGY CONSERVATION; FREE ENERGY; GLUCOSE; METABOLIC ENGINEERING; METABOLISM; PALMITIC ACID; STOICHIOMETRY; YEAST;

ACETYLATING ACETALDEHYDE DEHYDROGENASE; ATP-CITRATE LYASE; CARNITINE; PHOSPHOKETOLASE; PYRUVATE FORMATE LYASE; PYRUVATES;

PRODUCT DESIGN;

ACETYL COENZYME A; ALDEHYDE DEHYDROGENASE; BETA FARNESENE; BUTANOL; CARNITINE; CITRATE SYNTHASE; CITRIC ACID; FERREDOXIN; FLAVODOXIN; GLUCOSE; PALMITIC ACID; PHOSPHATE ACETYLTRANSFERASE; PHOSPHOKETOLASE; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATE OXIDASE; PYRUVIC ACID; UNCLASSIFIED DRUG; REACTIVE OXYGEN METABOLITE; SACCHAROMYCES CEREVISIAE PROTEIN;

CONTROLLED STUDY; CYTOSOL; ENZYME ENGINEERING; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SYNTHESIS; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; STOICHIOMETRY; THERMODYNAMICS; BIOSYNTHESIS; COENZYME; ENERGY METABOLISM; GENETIC ENHANCEMENT; GENETICS; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLISM; PHYSIOLOGY; PROCEDURES;

ACETYL COENZYME A; BIOSYNTHETIC PATHWAYS; COENZYMES; CYTOSOL; ENERGY METABOLISM; GENETIC ENHANCEMENT; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84961626309     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2016.03.006     Document Type: Review

References (154)

1. Aouida M., Rubio-Texeira M., Rubio Texeira M., Thevelein J.M., Poulin R., Ramotar D. Agp2, a member of the yeast amino acid permease family, positively regulates polyamine transport at the transcriptional level. PLoS One 2013, 8:e65717.
2. Avalos J.L., Fink G.R., Stephanopoulos G. Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat. Biotechnol. 2013, 31:335-341.
3. Bakker B.M., Overkamp K.M., Van Maris A.J.A., Kötter P., Luttik M.A.H., Van Dijken J.P., Pronk J.T. Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2001, 25:15-37.
4. Beekwilder J., Van Rossum H.M., Koopman F., Sonntag F., Buchhaupt M., Schrader J., Hall R.D., Bosch D., Pronk J.T., Van Maris A.J.A., Daran J.-M. Polycistronic expression of a β-carotene biosynthetic pathway in Saccharomyces cerevisiae coupled to β-ionone production. J. Biotechnol. 2014, 192:383-392.
5. Bekers, K.M., Heijnen, J.J., Van Gulik, W.M., 2015. Determination of the in vivo NAD:NADH ratio in Saccharomyces cerevisiae under anaerobic conditions, using alcohol dehydrogenase as sensor reaction. Yeast 32, 541-557.
6. Bieber L.L. Carnitine. Annu. Rev. Biochem. 1988, 57:261-283.
7. Bogorad I.W., Lin T.-S., Liao J.C. Synthetic non-oxidative glycolysis enables complete carbon conservation. Nature 2013, 502:693-697.
8. Boulton C.A., Ratledge C. Correlation of lipid accumulation in yeasts with possession of ATP:citrate lyase. Microbiology 1981, 127:169-176.
9. Branduardi P., Longo V., Berterame N.M., Rossi G., Porro D. A novel pathway to produce butanol and isobutanol in Saccharomyces cerevisiae. Biotechnol. Biofuels 2013, 6:68.
10. Brunengraber H., Lowenstein J.M. Effect of (-)-hydroxycitrate on ethanol metabolism. FEBS Lett. 1973, 36:130-132.
11. Buchanan B.B., Arnon D.I. A reverse KREBS cycle in photosynthesis: consensus at last. Photosynth. Res. 1990, 24:47-53.
12. Buu L.-M., Chen Y.-C., Lee F.-J.S. Functional characterization and localization of acetyl-CoA hydrolase, Ach1p, in Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278:17203-17209.
13. Canelas A.B., Van Gulik W.M., Heijnen J.J. Determination of the cytosolic free NAD/NADH ratio in Saccharomyces cerevisiae under steady-state and highly dynamic conditions. Biotechnol. Bioeng. 2008, 100:734-743.
14. Carlson R., Fell D., Srienc F. Metabolic pathway analysis of a recombinant yeast for rational strain development. Biotechnol. Bioeng. 2002, 79:121-134.
15. Caspi R., Altman T., Billington R., Dreher K., Foerster H., Fulcher C.A., Holland T.A., Keseler I.M., Kothari A., Kubo A., Krummenacker M., Latendresse M., Mueller L.A., Ong Q., Paley S., Subhraveti P., Weaver D.S., Weerasinghe D., Zhang P., Karp P.D. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res. 2014, 42:D459-D471.
16. Castegna A., Scarcia P., Agrimi G., Palmieri L., Rottensteiner H., Spera I., Germinario L., Palmieri F. Identification and functional characterization of a novel mitochondrial carrier for citrate and oxoglutarate in Saccharomyces cerevisiae. J. Biol. Chem. 2010, 285:17359-17370.
17. Chakrabarti A., Miskovic L., Soh K.C., Hatzimanikatis V. Towards kinetic modeling of genome-scale metabolic networks without sacrificing stoichiometric, thermodynamic and physiological constraints. Biotechnol. J. 2013, 8:1043-1057.
18. Chang A., Schomburg I., Placzek S., Jeske L., Ulbrich M., Xiao M., Sensen C.W., Schomburg D. BRENDA in 2015: exciting developments in its 25th year of existence. Nucleic Acids Res. 2014, 43:D439-D446.
19. Chantrenne H., Lipmann F. Coenzyme A dependence and acetyl donor function of the pyruvate-formate exchange system. J. Biol. Chem. 1950, 187:757-767.
20. Chen Y., Zhang Y., Siewers V., Nielsen J. Ach1 is involved in shuttling mitochondrial acetyl units for cytosolic C2 provision in Saccharomyces cerevisiae lacking pyruvate decarboxylase. FEMS Yeast Res. 2015, 15, fov015.
21. Choi J.W., Da Silva N.A. Improving polyketide and fatty acid synthesis by engineering of the yeast acetyl-CoA carboxylase. J. Biotechnol. 2014, 187:56-59.
22. Cronan J.E., Zhao X., Jiang Y. Function, attachment and synthesis of lipoic acid in Escherichia coli. Adv. Microb. Physiol. 2005, 50:103-146.
23. Cueto-Rojas H.F., Van Maris A.J.A., Wahl S.A., Heijnen J.J. Thermodynamics-based design of microbial cell factories for anaerobic product formation. Trends Biotechnol. 2015, 33:534-546.
24. Dandekar T., Schuster S., Snel B., Huynen M., Bork P. Pathway alignment: application to the comparative analysis of glycolytic enzymes. Biochem. J. 1999, 343(Pt 1):115-124.
25. De Jong B.W., Shi S., Siewers V., Nielsen J. Improved production of fatty acid ethyl esters in Saccharomyces cerevisiae through up-regulation of the ethanol degradation pathway and expression of the heterologous phosphoketolase pathway. Microb. Cell. Fact. 2014, 13:39.
26. De Kok S., Kozak B.U., Pronk J.T., Van Maris A.J.A. Energy coupling in Saccharomyces cerevisiae: selected opportunities for metabolic engineering. FEMS Yeast Res. 2012, 12:387-397.
27. DeLoache W.C., Russ Z.N., Narcross L., Gonzales A.M., Martin V.J.J., Dueber J.E. An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose. Nat. Chem. Biol. 2015, 11:465-471.
28. Dujon B., Sherman D., Fischer G., Durrens P., Casaregola S., Lafontaine I., De Montigny J., Marck C., Neuvéglise C., Talla E., Goffard N., Frangeul L., Aigle M., Anthouard V., Babour A., Barbe V., Barnay S., Blanchin S., Beckerich J.-M., Beyne E., Bleykasten C., Boisramé A., Boyer J., Cattolico L., Confanioleri F., De Daruvar A., Despons L., Fabre E., Fairhead C., Ferry-Dumazet H., Groppi A., Hantraye F., Hennequin C., Jauniaux N., Joyet P., Kachouri R., Kerrest A., Koszul R., Lemaire M., Lesur I., Ma L., Muller H., Nicaud J.-M., Nikolski M., Oztas S., Ozier-Kalogeropoulos O., Pellenz S., Potier S., Richard G.-F., Straub M.-L., Suleau A., Swennen D., Tekaia F., Wésolowski-Louvel M., Westhof E., Wirth B., Zeniou-Meyer M., Zivanovic I., Bolotin-Fukuhara M., Thierry A., Bouchier C., Caudron B., Scarpelli C., Gaillardin C., Weissenbach J., Wincker P., Souciet J.-L. Genome evolution in yeasts. Nature 2004, 430:35-44.
29. Elgersma Y., Van Roermund C.W., Wanders R.J., Tabak H.F. Peroxisomal and mitochondrial carnitine acetyltransferases of Saccharomyces cerevisiae are encoded by a single gene. EMBO J. 1995, 14:3472-3479.
30. Evans C.T., Ratledge C. Induction of xylulose-5-phosphate phosphoketolase in a variety of yeasts grown on d-xylose: the key to efficient xylose metabolism. Arch. Microbiol. 1984, 48-52.
31. Farhi M., Marhevka E., Masci T., Marcos E., Eyal Y., Ovadis M., Abeliovich H., Vainstein A. Harnessing yeast subcellular compartments for the production of plant terpenoids. Metab. Eng. 2011, 13:474-481.
32. Fatland B.L., Ke J., Anderson M.D., Mentzen W.I., Cui L.W., Allred C.C., Johnston J.L., Nikolau B.J., Wurtele E.S. Molecular characterization of a heteromeric ATP-citrate lyase that generates cytosolic acetyl-coenzyme A in Arabidopsis. Plant Physiol. 2002, 130:740-756.
33. Fendt S.-M., Sauer U. Transcriptional regulation of respiration in yeast metabolizing differently repressive carbon substrates. BMC Syst. Biol. 2010, 4:12.
34. Flamholz A., Noor E., Bar-Even A., Milo R. eQuilibrator - the biochemical thermodynamics calculator. Nucleic Acids Res. 2012, 40:770-775.
35. Fleck C.B., Brock M. Re-characterisation of Saccharomyces cerevisiae Ach1p: fungal CoA-transferases are involved in acetic acid detoxification. Fungal Genet. Biol. 2009, 46:473-485.
36. Flikweert M.T., De Swaaf M., Van Dijken J.P., Pronk J.T. Growth requirements of pyruvate-decarboxylase-negative Saccharomyces cerevisiae. FEMS Microbiol. Lett. 1999, 174:73-79.
37. Franken J., Kroppenstedt S., Swiegers J.H., Bauer F.F. Carnitine and carnitine acetyltransferases in the yeast Saccharomyces cerevisiae: a role for carnitine in stress protection. Curr. Genet. 2008, 53:347-360.
38. Gailiusis J., Rinne R.W., Benedict C.R. Pyruvate-oxaloacetate exchange reaction in Baker's yeast. Biochim. Biophys. Acta 1964, 92:595-601.
39. Galdieri L., Zhang T., Rogerson D., Lleshi R., Vancura A. Protein acetylation and acetyl coenzyme A metabolism in budding yeast. Eukaryot. Cell. 2014, 13:1472-1483.
40. Gancedo C. Inactivation of fructose-1,6-diphosphatase by glucose in yeast. J. Bacteriol. 1971, 107:401-405.
41. Gancedo J.M. Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 1998, 62:334-361.
42. Gancedo J.M., Gancedo C. Fructose-1, 6-diphosphatase, phosphofructokinase and glucose-6-phosphate dehydrogenase from fermenting and non fermenting yeasts. Arch. Microbiol. 1971, 138:132-138.
43. Gardner, T.S., Hawkins, K.M., Meadows, A.L., Tsong, A.E., Tsegaye, Y., 2013. Production of acetyl-coenzyme A derived isoprenoids. WO2013071172A1.
44. Geertman J.-M.A., Van Dijken J.P., Pronk J.T. Engineering NADH metabolism in Saccharomyces cerevisiae: Formate as an electron donor for glycerol production by anaerobic, glucose-limited chemostat cultures. FEMS Yeast Res. 2006, 6:1193-1203.
45. Guadalupe-Medina V., Wisselink H.W., Luttik M.A.H., De Hulster E., Daran J.-M., Pronk J.T., Van Maris A.J.A. Carbon dioxide fixation by Calvin-Cycle enzymes improves ethanol yield in yeast. Biotechnol. Biofuels 2013, 6:125.
46. Hawkins, K.M., Mahatdejkul-Meadows, T.T., Meadows, A.L., Pickens, L.B., Tai, A., Tsong, A.E., 2014. Use of phosphoketolase and phosphotransacetylase for production of acetyl-coenzyme a derived compounds. WO2014144135A3.
47. Heath E.C., Hurwitz J., Horecker B.L., Ginsburg A. Pentose fermentation by Lactobacillus plantarum. I. The cleavage of xylulose 5-phosphate by phosphoketolase. J. Biol. Chem. 1958, 231:1009-1029.
48. Heijnen J.J., Van Loosdrecht M.C.M., Tijhuis L. A black box mathematical model to calculate auto- and heterotrophic biomass yields based on Gibbs energy dissipation. Biotechnol. Bioeng. 1992, 40:1139-1154.
49. Henry C.S., Broadbelt L.J., Hatzimanikatis V. Thermodynamics-based metabolic flux analysis. Biophys. J. 2007, 92:1792-1805.
50. Hoelsch K., Sührer I., Heusel M., Weuster-Botz D. Engineering of formate dehydrogenase: Synergistic effect of mutations affecting cofactor specificity and chemical stability. Appl. Microbiol. Biotechnol. 2013, 97:2473-2481.
51. Hughes N.J., Clayton C.L., Chalk P.A., Kelly D.J. Helicobacter pylori porCDAB and oorDABC genes encode distinct pyruvate:flavodoxin and 2-oxoglutarate:acceptor oxidoreductases which mediate electron transport to NADP. J. Bacteriol. 1998, 180:1119-1128.
52. Huh W.-K., Falvo J.V., Gerke L.C., Carroll A.S., Howson R.W., Weissman J.S., O'Shea E.K. Global analysis of protein localization in budding yeast. Nature 2003, 425:686-691.
53. +-dependent pyruvate dehydrogenase in mitochondria of Euglena gracilis. J. Biochem. 1984, 96:931-934.
54. Inui H., Miyatake K., Nakano Y., Kitaoka S. Fatty acid synthesis in mitochondria of Euglena gracilis. Eur. J. Biochem. 1984, 142:121-126.
55. + oxidoreductase from Euglena gracilis: limited proteolysis of the enzyme with trypsin. Arch. Biochem. Biophys. 1991, 286:270-276.
56. Külzer R., Pils T., Kappl R., Hüttermann J., Knappe J. Reconstitution and characterization of the polynuclear iron-sulfur cluster in pyruvate formate-lyase-activating enzyme. Molecular properties of the holoenzyme form. J. Biol. Chem. 1998, 273:4897-4903.
57. Kandler O. Carbohydrate metabolism in lactic acid bacteria. Antonie van Leeuwenhoek 1983, 49:209-224.
58. Kanehisa M., Goto S., Sato Y., Kawashima M., Furumichi M., Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res. 2014, 42:199-205.
59. Khan A., Kolattukudy P.E. A microsomal fatty acid synthetase coupled to acyl-CoA reductase in Euglena gracilis. Arch. Biochem. Biophys. 1973, 158:411-420.
60. Kispal G., Cseko J., Alkonyi I., Sandor A. Isolation and characterization of carnitine acetyltransferase from S. cerevisiae. Biochim. Biophys. Acta 1991, 1085:217-222.
61. Knappe J., Blaschkowski H.P., Gröbner P., Schmitt T. Pyruvate formate-lyase of Escherichia coli: the acetyl-enzyme intermediate. Eur. J. Biochem. 1974, 50:253-263.
62. Knappe J., Schacht J., Möckel W., Höpner T., Vetter H., Edenharder R. Pyruvate formate-lyase reaction in Escherichia coli. the enzymatic system converting an inactive form of the lyase into the catalytically active enzyme. Eur. J. Biochem. 1969, 11:316-327.
63. Kocharin K., Siewers V., Nielsen J. Improved polyhydroxybutyrate production by Saccharomyces cerevisiae through the use of the phosphoketolase pathway. Biotechnol. Bioeng. 2013, 110:2216-2224.
64. Koh, J.L.Y., Chong, Y.T., Friesen, H., Moses, A., Boone, C., Andrews, B.J., Moffat, J., 2015. CYCLoPs: A comprehensive database constructed from automated analysis of protein abundance and subcellular localization patterns in Saccharomyces cerevisiae. G3 5, pp. 1223-1232.
65. Kohlhaw G.B., Tan-Wilson A. Carnitine acetyltransferase: Candidate for the transfer of acetyl groups through the mitochondrial membrane of yeast. J. Bacteriol. 1977, 129:1159-1161.
66. Koike M., Reed L.J., Carroll W.R. α-Keto acid dehydrogenation complexes. IV. Resolution and reconstitution of the Escherichia coli pyruvate dehydrogenation complex. J. Biol. Chem. 1963, 238:30-39.
67. 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. 2012, 11:155.
68. Kozak B.U., Van Rossum H.M., Benjamin K.R., Wu L., Daran J.-M.G., Pronk J.T., Van Maris A.J.A. Replacement of the Saccharomyces cerevisiae acetyl-CoA synthetases by alternative pathways for cytosolic acetyl-CoA synthesis. Metab. Eng. 2014, 21:46-59.
69. Kozak B.U., Van Rossum H.M., Niemeijer M.S., Van Dijk M., Benjamin K., Wu L., Daran J.-M.G., Pronk J.T., Van Maris A.J.A. Replacement of the initial steps of ethanol metabolism in Saccharomyces cerevisiae by ATP-independent acetylating acetaldehyde dehydrogenase. FEMS Yeast Res. 2016, 16. fow006.
70. Kozak B.U., Van Rossum H.M., Luttik M.A.H., Akeroyd M., Benjamin K.R., Wu L., De Vries S., Daran J.-M., Pronk J.T., Van Maris A.J.A. Engineering acetyl coenzyme A supply: Functional expression of a bacterial pyruvate dehydrogenase complex in the cytosol of Saccharomyces cerevisiae. mBio 2014, 5. e01696-14.
71. Krivoruchko A., Serrano-Amatriain C., Chen Y., Siewers V., Nielsen J. Improving biobutanol production in engineered Saccharomyces cerevisiae by manipulation of acetyl-CoA metabolism. J. Ind. Microbiol. Biotechnol. 2013, 40:1051-1056.
72. Krivoruchko A., Zhang Y., Siewers V., Chen Y., Nielsen J. Microbial acetyl-CoA metabolism and metabolic engineering. Metab. Eng. 2015, 28:28-42.
73. Leaf T.A., Peterson M.S., Stoup S.K., Somers D., Srienc F. Saccharomyces cerevisiae expressing bacterial polyhydroxybutyrate synthase produces poly-3-hydroxybutyrate. Microbiology 1996, 142:1169-1180.
74. Lian J., Zhao H. Recent advances in biosynthesis of fatty acids derived products in Saccharomyces cerevisiae via enhanced supply of precursor metabolites. J. Ind. Microbiol. Biotechnol. 2015, 42:437-451.
75. Lian J., Zhao H. Reversal of the β-oxidation cycle in Saccharomyces cerevisiae for production of fuels and chemicals. ACS Synth. Biol. 2015, 4:332-341.
76. Lian J., Si T., Nair N.U., Zhao H. Design and construction of acetyl-CoA overproducing Saccharomyces cerevisiae strains. Metab. Eng. 2014, 24:139-149.
77. Lipmann F. A phosphorylated oxidation product of pyruvic acid. J. Biol. Chem. 1940, 134:463-464.
78. 2 by heterotrophic bacteria. Annu. Rev. Microbiol. 1969, 23:515-538.
79. Lynd L.R., Wyman C.E., Gerngross T.U. Biocommodity engineering. Biotechnol. Prog. 1999, 15:777-793.
80. Mainguet S.E., Gronenberg L.S., Wong S.S., Liao J.C. A reverse glyoxylate shunt to build a non-native route from C4 to C2 in Escherichia coli. Metab. Eng. 2013, 19:116-127.
81. Mascal M. Chemicals from biobutanol: technologies and markets. Biofuels, Bioprod. Bioref. 2012, 6:483-493.
82. Max B., Salgado J.M., Rodríguez N., Cortés S., Converti A., Domínguez J.M. Biotechnological production of citric acid. Braz. J. Microbiol. 2010, 41:862-875.
83. + oxidoreductase and flavodoxin; key components of electron transfer in Escherichia coli. Eur. J. Biochem. 1998, 257:577-585.
84. Melnikov S., Ben-Shem A., Garreau de Loubresse N., Jenner L., Yusupova G., Yusupov M. One core, two shells: bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol. 2012, 19:560-567.
85. Miller C., Fosmer A., Rush B., McMullin T., Beacom D., Suominen P. Industrial production of lactic acid. Compr. Biotechnol. 2011, 179-188.
86. Navas M.a, Gancedo J.M. The regulatory characteristics of yeast fructose-1,6-bisphosphatase confer only a small selective advantage. J. Bacteriol. 1996, 178:1809-1812.
87. Nielsen J. Synthetic biology for engineering acetyl coenzyme A metabolism in yeast. MBio 2014, 5:e02153.
88. Nielsen J., Larsson C., Van Maris A.J.A., Pronk J.T. Metabolic engineering of yeast for production of fuels and chemicals. Curr. Opin. Biotechnol. 2013, 24:398-404.
89. Nielsen, J., Siewers, V., Kirvoruchko, A., Zhang, Y., Zhou, Y., Buds, N.A.A., Dai, Z., 2015. Engineering of acetyl-CoA metabolism in yeast. WO2015057154 A3.
90. Noor E., Haraldsdóttir H.S., Milo R., Fleming R.M.T. Consistent estimation of Gibbs energy using component contributions. PLoS Comput. Biol. 2013, 9:e1003098.
91. Oud B., Flores C.-L., Gancedo C., Zhang X., Trueheart J., Daran J.-M., Pronk J.T., Van Maris A.J.A. An internal deletion in MTH1 enables growth on glucose of pyruvate-decarboxylase negative, non-fermentative Saccharomyces cerevisiae. Microb. Cell. Fact. 2012, 11:131.
92. Oura E. The Effect of Aeration on the Growth Energetics and Biochemical Composition of Baker's Yeast 1972, University of Helsinki, Finland.
93. Overkamp K.M., Kötter P., Van der Hoek R., Schoondermark-Stolk S., Luttik Ma.H., Van Dijken J.P., Pronk J.T. Functional analysis of structural genes for NAD(+)-dependent formate dehydrogenase in Saccharomyces cerevisiae. Yeast 2002, 19:509-520.
94. Paddon C.J., Westfall P.J., Pitera D.J., Benjamin K., Fisher K., McPhee D., Leavell M.D., Tai A., Main A., Eng D., Polichuk D.R., Teoh K.H., Reed D.W., Treynor T., Lenihan J., Fleck M., Bajad S., Dang G., Dengrove D., Diola D., Dorin G., Ellens K.W., Fickes S., Galazzo J., Gaucher S.P., Geistlinger T., Henry R., Hepp M., Horning T., Iqbal T., Jiang H., Kizer L., Lieu B., Melis D., Moss N., Regentin R., Secrest S., Tsuruta H., Vazquez R., Westblade L.F., Xu L., Yu M., Zhang Y., Zhao L., Lievense J., Covello P.S., Keasling J.D., Reiling K.K., Renninger N.S., Newman J.D. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 2013, 496:528-532.
95. Palmieri L., Lasorsa F.M., Iacobazzi V., Runswick M.J., Palmieri F., Walker J.E. Identification of the mitochondrial carnitine carrier in Saccharomyces cerevisiae. FEBS Lett. 1999, 462:472-476.
96. Pel H.J., De Winde J.H., Archer D.B., Dyer P.S., Hofmann G., Schaap P.J., Turner G., De Vries R.P., Albang R., Albermann K., Andersen M.R., Bendtsen J.D., Benen Ja.E., Van den Berg M., Breestraat S., Caddick M.X., Contreras R., Cornell M., Coutinho P.M., Danchin E.G.J., Debets A.J.M., Dekker P., Van Dijck P.W.M., Van Dijk A., Dijkhuizen L., Driessen A.J.M., D'Enfert C., Geysens S., Goosen C., Groot G.S.P., De Groot P.W.J., Guillemette T., Henrissat B., Herweijer M., Van den Hombergh J.P.T.W., Van den Hondel C.A.M.J.J., Van der Heijden R.T.J.M., Van der Kaaij R.M., Klis F.M., Kools H.J., Kubicek C.P., Van Kuyk P.A., Lauber J., Lu X., Van der Maarel M.J.E.C., Meulenberg R., Menke H., Mortimer M.A., Nielsen J., Oliver S.G., Olsthoorn M., Pal K., Van Peij N.N.M.E., Ram A.F.J., Rinas U., Roubos J.A., Sagt C.M.J., Schmoll M., Sun J., Ussery D., Varga J., Vervecken W., Van de Vondervoort P.J.J., Wedler H., Wösten H.A.B., Zeng A.-P., Van Ooyen A.J.J., Visser J., Stam H. Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat. Biotechnol. 2007, 25:221-231.
97. Pokholok D.K., Harbison C.T., Levine S., Cole M., Hannett N.M., Lee T.I., Bell G.W., Walker K., Rolfe P.A., Herbolsheimer E., Zeitlinger J., Lewitter F., Gifford D.K., Young R.A. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 2005, 122:517-527.
98. Porro D., Brambilla L., Ranzi B.M., Martegani E., Alberghina L. Development of metabolically engineered Saccharomyces cerevisiae cells for the production of lactic acid. Biotechnol. Prog. 1995, 11:294-298.
99. Pronk J.T., Steensma H.Y., Van Dijken J.P. Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 1996, 12:1607-1633.
100. Pronk J.T., Wenzel T.J., Luttik M.A., Klaassen C.C., Scheffers W.A., Steensma H.Y., Van Dijken J.P. Energetic aspects of glucose metabolism in a pyruvate-dehydrogenase-negative mutant of Saccharomyces cerevisiae. Microbiology 1994, 140:601-610.
101. Przybyla-Zawislak B., Dennis R.A., Zakharkin S.O., McCammon M.T. Genes of succinyl-CoA ligase from Saccharomyces cerevisiae. Eur. J. Biochem. 1998, 258:736-743.
102. Ragsdale S.W. Pyruvate ferredoxin oxidoreductase and its radical intermediate. Chem. Rev. 2003, 103:2333-2346.
103. Ratledge C., Holdsworth J. Properties of a pentulose-5-phosphate phosphoketolase from yeasts grown on xylose. Appl. Microbiol. Biotechnol. 1985, 22:217-221.
104. Rodriguez S., Denby C.M., Van Vu T., Baidoo E.E.K., Wang G., Keasling J.D. ATP citrate lyase mediated cytosolic acetyl-CoA biosynthesis increases mevalonate production in Saccharomyces cerevisiae. Microb. Cell. Fact. 2016, 15:48.
105. + oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol. Biol. Evol. 2001, 18:710-720.
106. Rude M.A., Schirmer A. New microbial fuels: a biotech perspective. Curr. Opin. Microbiol. 2009, 12:274-281.
107. Ruijter G.J.G., Panneman H., Xu D.B., Visser J. Properties of Aspergillus niger citrate synthase and effects of citA overexpression on citric acid production. FEMS Microbiol. Lett. 2000, 184:35-40.
108. Ruiz-Amil M., De Torrontegui G., Palacián E., Catalina L., Losada M. Properties and function of yeast pyruvate carboxylase. J. Biol. Chem. 1965, 240:3485-3492.
109. Sánchez B.J., Nielsen J. Genome scale models of yeast: Towards standardized evaluation and consistent omic integration. Integr. Biol. 2015, 7:846-858.
110. Salusjarvi L., Kaunisto S., Holmstrom S., Vehkomaki M.L., Koivuranta K., Pitkanen J.P., Ruohonen L. Overexpression of NADH-dependent fumarate reductase improves D-xylose fermentation in recombinant Saccharomyces cerevisiae. J. Ind. Microbiol. Biotechnol. 2013, 40:1383-1392.
111. Sandoval C.M., Ayson M., Moss N., Lieu B., Jackson P., Gaucher S.P., Horning T., Dahl R.H., Denery J.R., Abbott D.A., Meadows A.L. Use of pantothenate as a metabolic switch increases the genetic stability of farnesene producing Saccharomyces cerevisiae. Metab. Eng. 2014, 25:1-12.
112. Sawers R.G. The hydrogenases and formate dehydrogenases of Escherichia coli. Antonie van Leeuwenhoek 1994, 66:57-88.
113. Schmalix W., Bandlow W. The ethanol-inducible YAT1 gene from yeast encodes a presumptive mitochondrial outer carnitine acetyltransferase. J. Biol. Chem. 1993, 268:27428-27439.
114. Schramm M., Racker E. Formation of erythrose-4-phosphate and acetyl phosphate by a phosphorolytic cleavage of fructose-6-phosphate. Nature 1957, 179:1349-1350.
115. Schramm M., Klybas V., Racker E. Phosphorolytic cleavage of fructose-6-phosphate by fructose-6-phosphate phosphoketolase from Acetobacter xylinum. J. Biol. Chem. 1958, 233:1283-1288.
116. Schuchmann K., Müller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat. Rev. Microbiol. 2014, 12:809-821.
117. Serov A.E., Popova A.S., Fedorchuk V.V., Tishkov V.I. Engineering of coenzyme specificity of formate dehydrogenase from Saccharomyces cerevisiae. Biochem. J. 2002, 367:841-847.
118. Sheng J., Feng X. Metabolic engineering of yeast to produce fatty acid-derived biofuels: bottlenecks and solutions. Front. Microbiol. 2015, 6:1-11.
119. Shiba Y., Paradise E.M., Kirby J., Ro D.-K., Keasling J.D. Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab. Eng. 2007, 9:160-168.
120. Snoep J.L., Westphal A.H., Benen J.A.E., Teixeira de Mattos M.J., Neijssel O.M., Kok A. Isolation and characterisation of the pyruvate dehydrogenase complex of anaerobically grown Enterococcus faecalis NCTC 775. Eur. J. Biochem. 1992, 203:245-250.
121. Snoep J.L., De Graef M.R., Westphal A.H., De Kok A., Teixeira de Mattos M.J., Neijssel O.M. Differences in sensitivity to NADH of purified pyruvate dehydrogenase complexes of Enterococcus faecalis, Lactococcus lactis, Azotobacter vinelandii and Escherichia coli: Implications for their activity in vivo. FEMS Microbiol. Lett. 1993, 114:279-283.
122. Soh K.C., Miskovic L., Hatzimanikatis V. From network models to network responses: integration of thermodynamic and kinetic properties of yeast genome-scale metabolic networks. FEMS Yeast Res. 2012, 12:129-143.
123. Sonderegger M., Schümperli M., Sauer U. Metabolic engineering of a phosphoketolase pathway for pentose catabolism in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2004, 70:2892-2897.
124. Stadtman E.R. The purification and properties of phosphotransacetylase. J. Biol. Chem. 1952, 196:527-534.
125. Stairs C.W., Roger A.J., Hampl V. Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a firmicute. Mol. Biol. Evol. 2011, 28:2087-2099.
126. Steen E.J., Chan R., Prasad N., Myers S., Petzold C.J., Redding A., Ouellet M., Keasling J.D. Metabolic engineering of Saccharomyces cerevisiae for the production of n-butanol. Microb. Cell. Fact. 2008, 7:36.
127. Strijbis K., Van Roermund C.W.T., Hardy G.P., Van den Burg J., Bloem K., De Haan J., Van Vlies N., Wanders R.J.A., Vaz F.M., Distel B. Identification and characterization of a complete carnitine biosynthesis pathway in Candida albicans. FASEB J. 2009, 23:2349-2359.
128. Sutendra G., Kinnaird A., Dromparis P., Paulin R., Stenson T.H., Haromy A., Hashimoto K., Zhang N., Flaim E., Michelakis E.D. A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 2014, 158:84-97.
129. Swidah R., Wang H., Reid P.J., Ahmed H.Z., Pisanelli A.M., Persaud K.C., Grant C.M., Ashe M.P. Butanol production in S. cerevisiae via a synthetic ABE pathway is enhanced by specific metabolic engineering and butanol resistance. Biotechnol. Biofuels 2015, 8:97.
130. Swiegers J.H., Dippenaar N., Pretorius I.S., Bauer F.F. Carnitine-dependent metabolic activities in Saccharomyces cerevisiae: three carnitine acetyltransferases are essential in a carnitine-dependent strain. Yeast 2001, 18:585-595.
131. Tang X., Feng H., Chen W.N. Metabolic engineering for enhanced fatty acids synthesis in Saccharomyces cerevisiae. Metab. Eng. 2013, 16:95-102.
132. Tehlivets O., Scheuringer K., Kohlwein S.D. Fatty acid synthesis and elongation in yeast. Biochim. Biophys. Acta 2007, 1771:255-270.
133. Thykaer J., Nielsen J. Evidence, through C13-labelling analysis, of phosphoketolase activity in fungi. Process. Biochem. 2007, 42:1050-1055.
134. Tittmann K., Wille G., Golbik R., Weidner A., Ghisla S., Hübner G. Radical phosphate transfer mechanism for the thiamin diphosphate- and FAD-dependent pyruvate oxidase from Lactobacillus plantarum. Kinetic coupling of intercofactor electron transfer with phosphate transfer to acetyl-thiamin diphosphate via a trans. Biochemistry 2005, 44:13291-13303.
135. Tucci S., Vacula R., Krajcovic J., Proksch P., Martin W. Variability of wax ester fermentation in natural and bleached Euglena gracilis strains in response to oxygen and the elongase inhibitor flufenacet. J. Eukaryot. Microbiol. 2010, 57:63-69.
136. Van den Berg M.A., Steensma H.Y. ACS2, a Saccharomyces cerevisiae gene encoding acetyl-coenzyme A synthetase, essential for growth on glucose. Eur. J. Biochem. 1995, 231:704-713.
137. Van Maris A.J.A., Luttik M.A.H., Winkler A.A., Van Dijken J.P., Pronk J.T. Overproduction of threonine aldolase circumvents the biosynthetic role of pyruvate decarboxylase in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2003, 69:2094-2099.
138. Van Maris A.J.A., Winkler A.A., Porro D., Van Dijken J.P., Pronk J.T. Homofermentative lactate production cannot sustain anaerobic growth of engineered Saccharomyces cerevisiae: possible consequence of energy-dependent lactate export. Appl. Environ. Microbiol. 2004, 70:2898-2905.
139. 2-independent, glucose-tolerant, and pyruvate-hyperproducing yeast. Appl. Environ. Microbiol. 2004, 70:159-166.
140. Van Roermund C.W., Elgersma Y., Singh N., Wanders R.J., Tabak H.F. The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J. 1995, 14:3480-3486.
141. Van Roermund C.W., Hettema E.H., Van den Berg M., Tabak H.F., Wanders R.J. Molecular characterization of carnitine-dependent transport of acetyl-CoA from peroxisomes to mitochondria in Saccharomyces cerevisiae and identification of a plasma membrane carnitine transporter, Agp2p. EMBO J. 1999, 18:5843-5852.
142. Van Rossum H.M., Kozak B.U., Niemeijer M.S., Duine H.J., Luttik M.A.H., Boer V.M., Kötter P., Daran J.-M.G., Van Maris A.J.A., Pronk J.T. Alternative reactions at the interface of glycolysis and citric acid cycle in Saccharomyces cerevisiae. FEMS Yeast Res. 2016, fow017.
143. Van Rossum, H.M., Kozak, B.U., Niemeijer, M.S., Dykstra, J.C., Luttik, M.A.H., Daran, J.-M.G., Van Maris, A.J.A., Pronk, J.T., 2016b. Requirements for carnitine-shuttle-mediated translocation of mitochondrial acetyl moieties to the yeast cytosol. (Unpublished results).
144. Vax F.M., Wanders R.J.A. Carnitine biosynthesis in mammals. Biochem. J. 2002, 361:417.
145. Verduyn C., Stouthamer A.H, Scheffers W.A, Van Dijken J.P A theoretical evaluation of growth yields of yeasts Antonie van Leeuwenhoek 1991, 59:49-63.
146. Verwaal R., Wang J., Meijnen J.P., Visser H., Sandmann G., Van Den Berg J.A., Van Ooyen A.J.J. High-level production of beta-carotene in Saccharomyces cerevisiae by successive transformation with carotenogenic genes from Xanthophyllomyces dendrorhous. Appl. Environ. Microbiol. 2007, 73:4342-4350.
147. Von Kamp A., Schuster S. Metatool 5.0: fast and flexible elementary modes analysis. Bioinformatics 2006, 22:1930-1931.
148. Waks Z., Silver P.A. Engineering a synthetic dual-organism system for hydrogen production. Appl. Environ. Microbiol. 2009, 75:1867-1875.
149. Weusthuis R.A., Lamot I., Van der Oost J., Sanders J.P.M. Microbial production of bulk chemicals: Development of anaerobic processes. Trends Biotechnol. 2011, 29:153-158.
150. Yan D., Wang C., Zhou J., Liu Y., Yang M., Xing J. Construction of reductive pathway in Saccharomyces cerevisiae for effective succinic acid fermentation at low pH value. Bioresour. Technol. 2014, 156:232-239.
151. Zelle R.M., De Hulster E., Van Winden W.A., De Waard P., Dijkema C., Winkler A.A., Geertman J.-M.A., Van Dijken J.P., Pronk J.T., Van Maris A.J.A. Malic acid production by Saccharomyces cerevisiae: engineering of pyruvate carboxylation, oxaloacetate reduction, and malate export. Appl. Environ. Microbiol. 2008, 74:2766-2777.
152. Zhang J., Pierick A., ten, Van Rossum H.M., Maleki Seifar R., Ras C., Daran J.-M., Heijnen J.J., Aljoscha Wahl S. Determination of the cytosolic NADPH/NADP ratio in Saccharomyces cerevisiae using shikimate dehydrogenase as sensor reaction. Sci. Rep. 2015, 5:12846.
153. Zhang Y., Dai Z., Krivoruchko A., Chen Y., Siewers V., Nielsen J. Functional pyruvate formate lyase pathway expressed with two different electron donors in Saccharomyces cerevisiae at aerobic growth. FEMS Yeast Res. 2015, 15. fov024.
154. Zhou Z.H., McCarthy D.B., O'Connor C.M., Reed L.J., Stoops J.K. The remarkable structural and functional organization of the eukaryotic pyruvate dehydrogenase complexes. Proc. Natl. Acad. Sci. USA 2001, 98:14802-14807.