Engineering acetyl coenzyme a supply: Functional expression of a bacterial pyruvate dehydrogenase complex in the cytosol of Saccharomyces cerevisiae

mBio

Volumn 5, Issue 5, 2014, Pages

  Kozak, Barbara U ^a   van Rossum, Harmen M ^a   Luttik, Marijke A H ^a   Akeroyd, Michiel ^c   Benjamin, Kirsten R ^b   Wu, Liang ^c   de Vries, Simon ^a   Daran, Jean Marc ^a   Pronk, Jack T ^a   van Maris, Antonius J A ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b Amyris Inc   (United States)

^c DSM BIOTECHNOLOGY CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A; ADENOSINE TRIPHOSPHATE; GLUCOSE; PYRUVATE DEHYDROGENASE COMPLEX; THIOCTIC ACID; BACTERIAL PROTEIN; CULTURE MEDIUM; RECOMBINANT PROTEIN;

AEROBIC CELL CULTURE; ANAEROBIC CELL CULTURE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BIOMASS; CELL FRACTIONATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOSOL; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME PURIFICATION; ENZYME SUBUNIT; ENZYME SYNTHESIS; GEL FILTRATION; GENE EXPRESSION; IN VIVO STUDY; LIPOYLATION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; STRAIN DIFFERENCE; WILD TYPE; AEROBIC METABOLISM; ANAEROBIC GROWTH; CHEMISTRY; DNA SEQUENCE; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLISM; MOLECULAR GENETICS;

BACTERIA (MICROORGANISMS); SACCHAROMYCES CEREVISIAE;

ACETYL COENZYME A; AEROBIOSIS; ANAEROBIOSIS; BACTERIAL PROTEINS; BIOMASS; CULTURE MEDIA; CYTOSOL; ENTEROCOCCUS FAECALIS; GENE EXPRESSION PROFILING; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; MOLECULAR SEQUENCE DATA; PYRUVATE DEHYDROGENASE COMPLEX; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA;

EID: 84908409797     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01696-14     Document Type: Article

References (68)

1. Patel MS, Roche TE. 1990. Molecular biology and biochemistry of pyruvate dehydrogenase complexes. FASEB J. 4:3224-3233.
2. Domingo GJ, Chauhan HJ, Lessard IA, Fuller C, Perham RN. 1999. Self-assembly and catalytic activity of the pyruvate dehydrogenase multienzyme complex from Bacillus stearothermophilus. Eur. J. Biochem. 266: 1136-1146. http://dx.doi.org/10.1046/j.1432-1327.1999.00966.x.
3. Perham RN, Hooper EA. 1977. Polypeptide chain stoichiometry in the self-assembly of the pyruvate dehydrogenase multienzyme complex of Escherichia coli. FEBS Lett. 73:137-140. http://dx.doi.org/10.1016/0014- 5793(77)80965-4.
4. Witzmann S, Bisswanger H. 1998. The pyruvate dehydrogenase complex from thermophilic organisms: thermal stability and re-association from the enzyme components. Biochim. Biophys. Acta 1385:341-352. http:// dx.doi.org/10.1016/S0167-4838(98)00078-8.
5. Chen Y, Bao J, Kim IK, Siewers V, Nielsen J. 2014. Coupled incremental precursor and co-factor supply impr 3-hydroxypropionic acid production in Saccharomyces cerevisiae. Metab. Eng. 22:104-109. http://dx.doi.org/ 10.1016/j.ymben.2014.01.005.
6. Dyer JM, Chapital DC, Kuan JW, Mullen RT, Pepperman AB. 2002. Metabolic engineering of Saccharomyces cerevisiae for production of novel lipid compounds. Appl. Microbiol. Biotechnol. 59:224 -230. http:// dx.doi.org/10.1007/s00253-002-0997-5.
7. Koopman F, Beekwilder J, Crimi B, van Houwelingen A, Hall RD, Bosch D, van Maris AJ, Pronk JT, Daran JM. 2012. De novo production of the flavonoid naringenin in engineered Saccharomyces cerevisiae. Microb. Cell Fact. 11:155. http://dx.doi.org/10.1186/1475-2859-11-155.
8. Shiba Y, Paradise EM, Kirby J, Ro DK, Keasling JD. 2007. Engineering of the pyruvate dehydrogenase bypass in Saccharomyces cerevisiae for high-level production of isoprenoids. Metab. Eng. 9:160 -168. http:// dx.doi.org/10.1016/j.ymben.2006.10.005.
9. Steen EJ, Chan R, Prasad N, Myers S, Petzold CJ, Redding A, Ouellet M, Keasling JD. 2008. Metabolic engineering of Saccharomyces cerevisiae for the production of n-butanol. Microb. Cell Fact. 7:36. http:// dx.doi.org/10.1186/1475-2859-7-36.
10. Veen M, Lang C. 2004. Production of lipid compounds in the yeast Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 63:635- 646. http://dx.doi.org/10.1007/s00253-003-1456-7.
11. Hong KK, Nielsen J. 2012. Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries. Cell. Mol. Life Sci. 69:2671-2690. http://dx.doi.org/10.1007/s00018-012-0945-1.
12. Pronk JT, Yde Steensma H, van Dijken JP. 1996. Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 12:1607-1633. http://dx.doi.org/ 10.1002/(SICI)1097-0061(199612)12:16+1607::AID-YEA70+3.0.CO; 2-4.
13. Avalos JL, Fink GR, Stephanopoulos G. 2013. Compartmentalization of metabolic pathways in yeast mitochondria improves the production of branched-chain alcohols. Nat. Biotechnol. 31:335-341. http://dx.doi.org/ 10.1038/nbt.2509.
14. Chen Y, Daviet L, Schalk M, Siewers V, Nielsen J. 2013. Establishing a platform cell factory through engineering of yeast acetyl-CoA metabolism. Metab. Eng. 15:48-54. http://dx.doi.org/10.1016/j.ymben.2012.11.002.
15. Kocharin K, Siewers V, Nielsen J. 2013. Improved polyhydroxybutyrate production by Saccharomyces cerevisiae through the use of the phosphoketolase pathway. Biotechnol. Bioeng. 110:2216-2224. http://dx.doi.org/ 10.1002/bit.24888.
16. Krivoruchko A, Serrano-Amatriain C, Chen Y, Siewers V, Nielsen J. 2013. Improving biobutanol production in engineered Saccharomyces cerevisiae by manipulation of acetyl-CoA metabolism. J. Ind. Microbiol. Biotechnol. 40:1051-1056. http://dx.doi.org/10.1007/s10295-013- 1296-0.
17. Tang X, Feng H, Chen WN. 2013. Metabolic engineering for enhanced fatty acids synthesis in Saccharomyces cerevisiae. Metab. Eng. 16:95-102. http://dx.doi.org/10.1016/j.ymben.2013.01.003.
18. Kozak BU, van Rossum HM, Benjamin KR, Wu L, Daran JM, Pronk JT, van Maris AJ. 2014. Replacement of the Saccharomyces cerevisiae acetyl-CoA synthetases by alternative pathways for cytosolic acetyl-CoA synthesis. Metab. Eng. 21:46 -59. http://dx.doi.org/10.1016/ j.ymben.2013.11.005.
19. Snoep JL, de Graef MR, Westphal AH, de Kok A, Teixeira de Mattos MJ, Neijssel OM. 1993. 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. 114:279-283. http://dx.doi.org/ 10.1111/j.1574-6968.1993.tb06586.x.
20. Snoep JL, Westphal AH, Benen JA, Teixeira de Mattos MJ, Neijssel OM, de Kok A. 1992. Isolation and characterisation of the pyruvate dehydrogenase complex of anaerobically grown Enterococcus faecalis NCTC 775. Eur. J. Biochem. 203:245-250. http://dx.doi.org/10.1111/j.1432- 1033.1992.tb19853.x.
21. Canelas AB, van Gulik WM, Heijnen JJ. 2008. Determination of the cytosolic free NAD/NADH ratio in Saccharomyces cerevisiae under steadystate and highly dynamic conditions. Biotechnol. Bioeng. 100:734-743. http://dx.doi.org/10.1002/bit.21813.
22. Cronan JE, Zhao X, Jiang Y. 2005. Function, attachment and synthesis of lipoic acid in Escherichia coli. Adv. Microb. Physiol. 50:103-146. http:// dx.doi.org/10.1016/S0065-2911(05)50003-1.
23. Hermes FA, Cronan JE. 2013. The role of the Saccharomyces cerevisiae lipoate protein ligase homologue, Lip3, in lipoic acid synthesis. Yeast 30: 415-427.
24. Martin N, Christensen QH, Mansilla MC, Cronan JE, de Mendoza D. 2011. A novel two-gene requirement for the octanoyltransfer reaction of Bacillus subtilis lipoic acid biosynthesis. Mol. Microbiol. 80:335-349. http://dx.doi.org/10.1111/j.1365-2958.2011.07597.x.
25. De Virgilio C, Burckert N, Barth G, Neuhaus JM, Boller T, Wiemken A. 1992. Cloning and disruption of a gene required for growth on acetate but not on ethanol: the acetyl-coenzyme A synthetase gene of Saccharomyces cerevisiae. Yeast 8:1043-1051. http://dx.doi.org/10.1002/yea.320081207.
26. van den Berg MA, Steensma HY. 1995. ACS2, a Saccharomyces cerevisiae gene encoding acetyl-coenzyme A synthetase, essential for growth on glucose. Eur. J. Biochem. 231:704 -713. http://dx.doi.org/10.1111/j.1432- 1033.1995.tb20751.x.
27. de Jong-Gubbels P, van den Berg MA, Steensma HY, van Dijken JP, Pronk JT. 1997. The Saccharomyces cerevisiae acetyl-coenzyme A synthetase encoded by the ACS1 gene, but not the ACS2-encoded enzyme, is subject to glucose catabolite inactivation. FEMS Microbiol. Lett. 153: 75-81. http://dx.doi.org/10.1016/S0378-1097(97)00236-X.
28. van den Berg MA, de Jong-Gubbels P, Kortland CJ, van Dijken JP, Pronk JT, Steensma HY. 1996. The two acetyl-coenzyme A synthetases of Saccharomyces cerevisiae differ with respect to kinetic properties and transcriptional regulation. J. Biol. Chem. 271:28953-28959. http://dx.doi.org/ 10.1074/jbc.271.46.28953.
29. Luttik MA, Overkamp KM, Kötter P, de Vries S, van Dijken JP, Pronk JT. 1998. The Saccharomyces cerevisiae NDE1 and NDE2 genes encode separate mitochondrial NADH dehydrogenases catalyzing the oxidation of cytosolic NADH. J. Biol. Chem. 273:24529-24534. http://dx.doi.org/ 10.1074/jbc.273.38.24529.
30. Henriksen P, Wagner SA, Weinert BT, Sharma S, Bacinskaja G, Rehman M, Juffer AH, Walther TC, Lisby M, Choudhary C. 2012. Proteome-wide analysis of lysine acetylation suggests its broad regulatory scope in Saccharomyces cerevisiae. Mol. Cell. Proteomics 11:1510-1522. http://dx.doi.org/10.1074/mcp.M112.017251.
31. Lin YY, Lu JY, Zhang J, Walter W, Dang W, Wan J, Tao SC, Qian J, Zhao Y, Boeke JD, Berger SL, Zhu H. 2009. Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136:1073-1084. http://dx.doi.org/10.1016/j.cell.2009.01.033.
32. Lu JY, Lin YY, Sheu JC, Wu JT, Lee FJ, Chen Y, Lin MI, Chiang FT, Tai TY, Berger SL, Zhao Y, Tsai KS, Zhu H, Chuang LM, Boeke JD. 2011. Acetylation of yeast AMPK controls intrinsic aging independently of caloric restriction. Cell 146:969 -979. http://dx.doi.org/10.1016/ j.cell.2011.07.044.
33. Shi L, Tu BP. 2013. Acetyl-CoA induces transcription of the key G1 cyclin CLN3 to promote entry into the cell division cycle in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 110:7318 -7323. http://dx.doi.org/ 10.1073/pnas.1302490110.
34. Weinert BT, Iesmantavicius V, Moustafa T, Schölz C, Wagner SA, Magnes C, Zechner R, Choudhary C. 2014. Acetylation dynamics and stoichiometry in Saccharomyces cerevisiae. Mol. Syst. Biol. 10:716. http:// dx.doi.org/10.1002/msb.134766.
35. Takahashi H, McCaffery JM, Irizarry RA, Boeke JD. 2006. Nucleocytosolic acetyl-coenzyme A synthetase is required for histone acetylation and global transcription. Mol. Cell 23:207-217. http://dx.doi.org/10.1016/ j.molcel.2006.05.040.
36. Huggett J, Dheda K, Bustin S, Zumla A. 2005. Real-time RT-PCR normalisation; strategies and considerations. Genes Immun. 6:279-284. http://dx.doi.org/10.1038/sj.gene.6364190.
37. Marvin ME, Williams PH, Cashmore AM. 2001. The isolation and characterisation of a Saccharomyces cerevisiae gene (LIP2) involved in the attachment of lipoic acid groups to mitochondrial enzymes. FEMS Microbiol. Lett. 199:131-136. http://dx.doi.org/10.1111/j.1574- 6968.2001.tb10663.x.
38. Sulo P, Martin NC. 1993. Isolation and characterization of LIP5. A lipoate biosynthetic locus of Saccharomyces cerevisiae. J. Biol. Chem. 268: 17634-17639.
39. Schonauer MS, Kastaniotis AJ, Kursu VA, Hiltunen JK, Dieckmann CL. 2009. Lipoic acid synthesis and attachment in yeast mitochondria. J. Biol. Chem. 284:23234-23242. http://dx.doi.org/10.1074/jbc.M109.015594.
40. Lian J, Si T, Nair NU, Zhao H. 2014. Design and construction of acetyl-CoA overproducing Saccharomyces cerevisiae strains. Metab. Eng. 24:139-149. http://dx.doi.org/10.1016/j.ymben.2014.05.010.
41. Bates DL, Danson MJ, Hale G, Hooper EA, Perham RN. 1977. Selfassembly and catalytic activity of the pyruvate dehydrogenase multienzyme complex of Escherichia coli. Nature 268:313-316. http://dx.doi.org/ 10.1038/268313a0.
42. Izard T, Sarfaty S, Westphal A, de Kok A, Hol WG. 1997. Improvement of diffraction quality upon rehydration of dehydrated icosahedral Enterococcus faecalis pyruvate dehydrogenase core crystals. Protein Sci. 6:913-915.
43. Wilkinson KD, Williams CH, Jr. 1981. NADH inhibition and NAD activation of Escherichia coli lipoamide dehydrogenase catalyzing the NADH-lipoamide reaction. J. Biol. Chem. 256:2307-2314.
44. Sonderegger M, Schümperli M, Sauer U. 2004. Metabolic engineering of a phosphoketolase pathway for pentose catabolism in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 70:2892-2897. http://dx.doi.org/ 10.1128/AEM.70.5.2892-2897.2004.
45. Entian KD, Kotter P. 2007. 25 yeast genetic strain and plasmid collections. Methods Mol. Biol. 36:629-666.
46. Nijkamp JF, van den Broek M, Datema E, de Kok S, Bosman L, Luttik MA, Daran-Lapujade P, Vongsangnak W, Nielsen J, Heijne WH, Klaassen P, Paddon CJ, Platt D, Kotter P, van Ham RC, Reinders MJ, Pronk JT, de Ridder D, Daran JM. 2012. De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microb. Cell Fact. 11:36. http://dx.doi.org/10.1186/1475-2859-11-36.
47. 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. http://dx.doi.org/10.1002/yea.320080703.
48. Pronk JT. 2002. Auxotrophic yeast strains in fundamental and applied research. Appl. Environ. Microbiol. 68:2095-2100. http://dx.doi.org/ 10.1128/AEM.68.5.2095-2100.2002.
49. Roubos JA, v. Peij NNME. 2008. A method for achieving improved polypeptide expression. International patent WO/2008/000632.
50. Kuijpers NG, Solis-Escalante D, Bosman L, van den Broek M, Pronk JT, Daran JM, Daran-Lapujade P. 2013. A versatile, efficient strategy for assembly of multi-fragment expression vectors in Saccharomyces cerevisiae using 60-bp synthetic recombination sequences. Microb. Cell Fact. 12:47. http://dx.doi.org/10.1186/1475-2859-12-47.
51. Gietz RD, Woods RA. 2002. Transformation of yeast by lithium acetate/ single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350:87-96. http://dx.doi.org/10.1016/S0076-6879(02)50957-5.
52. Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH. 2002. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30:e23. http://dx.doi.org/ 10.1093/nar/30.6.e23.
53. Oud B, Flores CL, Gancedo C, Zhang X, Trueheart J, Daran JM, Pronk JT, van Maris AJ. 2012. An internal deletion in MTH1 enables growth on glucose of pyruvate-decarboxylase negative, non-fermentative Saccharomyces cerevisiae. Microb. Cell Fact. 11:131. http://dx.doi.org/10.1186/ 1475-2859-11-131.
54. de Kok S, Yilmaz D, Suir E, Pronk JT, Daran JM, van Maris AJ. 2011. Increasing free-energy (ATP) conservation in maltose-grown Saccharomyces cerevisiae by expression of a heterologous maltose phosphorylase. Metab. Eng. 13:518-526. http://dx.doi.org/10.1016/j.ymben.2011.06.001.
55. Guadalupe Medina V, Almering MJ, van Maris AJ, Pronk JT. 2010. Elimination of glycerol production in anaerobic cultures of a Saccharomyces cerevisiae strain engineered to use acetic acid as an electron acceptor. Appl. Environ. Microbiol. 76:190 -195. http://dx.doi.org/10.1128/ AEM.01772-09.
56. Mashego MR, van Gulik WM, Vinke JL, Heijnen JJ. 2003. Critical evaluation of sampling techniques for residual glucose determination in carbon-limited chemostat culture of Saccharomyces cerevisiae. Biotechnol. Bioeng. 83:395-399. http://dx.doi.org/10.1002/bit.10683.
57. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
58. Flikweert MT, van Dijken JP, Pronk JT. 1997. Metabolic responses of pyruvate decarboxylase-negative Saccharomyces cerevisiae to glucose excess. Appl. Environ. Microbiol. 63:3399-3404.
59. Wenzel TJ, van den Berg MA, Visser W, van den Berg JA, Steensma HY. 1992. Characterization of Saccharomyces cerevisiae mutants lacking the E1+ subunit of the pyruvate dehydrogenase complex. Eur. J. Biochem. 209:697-705. http://dx.doi.org/10.1111/j.1432-1033.1992.tb17338.x.
60. Vogel O, Beikirch H, Muller H, Henning U. 1971. The subunit structure of the Escherichia coli K-12 pyruvate dehydrogenase complex. The dihydrolipoamide transacetylase component. Eur. J. Biochem. 20:169-178. http://dx.doi.org/10.1111/j.1432-1033.1971.tb01375.x.
61. de Jonge LP, Buijs NA, ten Pierick A, Deshmukh A, Zhao Z, Kiel JA, Heijnen JJ, van Gulik WM. 2011. Scale-down of penicillin production in Penicillium chrysogenum. Biotechnol. J. 6:944 -958. http://dx.doi.org/ 10.1002/biot.201000409.
62. Lu P, Vogel C, Wang R, Yao X, Marcotte EM. 2007. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25:117-124. http:// dx.doi.org/10.1038/nbt1270.
63. Hazelwood LA, Walsh MC, Pronk JT, Daran JM. 2010. Involvement of vacuolar sequestration and active transport in tolerance of Saccharomyces cerevisiae to hop iso-_-acids. Appl. Environ. Microbiol. 76:318 -328. http://dx.doi.org/10.1128/AEM.01457-09.
64. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754 -1760. http:// dx.doi.org/10.1093/bioinformatics/btp324.
65. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28:-511-515. http:// dx.doi.org/10.1038/nbt.1621.
66. Knijnenburg TA, de Winde JH, Daran JM, Daran-Lapujade P, Pronk JT, Reinders MJ, Wessels LF. 2007. Exploiting combinatorial cultivation conditions to infer transcriptional regulation. BMC Genomics 8:25. http://dx.doi.org/10.1186/1471-2164-8-25.
67. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122. http://dx.doi.org/10.1016/0378-1119(92)90454-W.
68. Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.