PHO13 deletion-induced transcriptional activation prevents sedoheptulose accumulation during xylose metabolism in engineered Saccharomyces cerevisiae

Metabolic Engineering

Volumn 34, Issue , 2016, Pages 88-96

  Xu, Haiqing ^a   Kim, Sooah ^b   Sorek, Hagit ^c   Lee, Yongsuk ^d   Jeong, Dukyeol ^d   Kim, Jungyeon ^b   Oh, Eun Joong ^a   Yun, Eun Ju ^b   Wemmer, David E ^c   Kim, Kyoung Heon ^b   Kim, Soo Rin ^d   Jin, Yong Su ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b Korea University   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Kyungpook National University   (South Korea)

Author keywords

Cas9 guided genome editing technique; GC TOF MS; Metabolomics; NMR; RNA seq

Indexed keywords

CARBON; CHEMICAL ACTIVATION; ENCODING (SYMBOLS); METABOLISM; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; YEAST;

CAS9-GUIDED GENOME EDITING TECHNIQUE; GC-TOF/MS; INTRACELLULAR METABOLITES; METABOLOMICS; PENTOSE PHOSPHATE PATHWAY; TRANSCRIPTIONAL ACTIVATIONS; TRANSCRIPTIONAL CHANGES; XYLOSE FERMENTATION;

METABOLIC ENGINEERING;

PHO13 ENZYME; PHOSPHATASE; TRANSALDOLASE; UNCLASSIFIED DRUG; XYLOSE; HEPTOSE; PHO13 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SEDOHEPTULOSE;

ARTICLE; CARBOHYDRATE METABOLISM; DEPHOSPHORYLATION; GENE DELETION; HETERONUCLEAR MULTIPLE BOND CORRELATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION; TRANSGENIC ORGANISM; ENZYME ACTIVATION; GENE SILENCING; GENETIC ENHANCEMENT; GENETICS; METABOLIC ENGINEERING; METABOLISM; PHYSIOLOGY; PROCEDURES;

ENZYME ACTIVATION; GENE SILENCING; GENETIC ENHANCEMENT; HEPTOSES; METABOLIC ENGINEERING; PHOSPHORIC MONOESTER HYDROLASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTIONAL ACTIVATION; XYLOSE;

EID: 84953774938     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2015.12.007     Document Type: Article

References (60)

1. Billard P., Menart S., Fleer R., Bolotinfukuhara M. Isolation and characterization of the gene encoding xylose reductase from Kluyveromyces Lactis. Gene 1995, 162:93-97.
2. Brat D., Boles E., Wiedemann B. Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2009, 75:2304-2311.
3. Ceusters J., Godts C., Peshev D., Vergauwen R., Dyubankova N., Lescrinier E., De Proft M.P., Van den Ende W. Sedoheptulose accumulation under CO2 enrichment in leaves of Kalanchoe pinnata: a novel mechanism to enhance C and P homeostasis?. J. Exp. Bot. 2013, 64:1497-1507.
4. Denkert C., Budczies J., Weichert W., Wohlgemuth G., Scholz M., Kind T., Niesporek S., Noske A., Buckendahl A., Dietel M., Fiehn O. Metabolite profiling of human colon carcinoma--deregulation of TCA cycle and amino acid turnover. Mol. Cancer. 2008, 7:72.
5. Diao L., Liu Y., Qian F., Yang J., Jiang Y., Yang S. Construction of fast xylose-fermenting yeast based on industrial ethanol-producing diploid Saccharomyces cerevisiae by rational design and adaptive evolution. BMC Biotechnol. 2013, 13:110.
6. DiCarlo J.E., Norville J.E., Mali P., Rios X., Aach J., Church G.M. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 2013, 41:4336-4343.
7. Dromms R.A., Styczynski M.P. Systematic applications of metabolomics in metabolic engineering. Metabolites 2012, 2:1090-1122.
8. Farwick A., Bruder S., Schadeweg V., Oreb M., Boles E. Engineering of yeast hexose transporters to transport D-xylose without inhibition by D-glucose. Proc. Natl. Acad. Sci. U. S. A 2014, 111:5159-5164.
9. Fujitomi K., Sanda T., Hasunuma T., Kondo A. Deletion of the PHO13 gene in Saccharomyces cerevisiae improves ethanol production from lignocellulosic hydrolysate in the presence of acetic and formic acids, and furfural. Bioresour. Technol. 2012, 111:161-166.
10. Hahn-Hagerdal B., Karhumaa K., Jeppsson M., Gorwa-Grauslund M.F. Metabolic engineering for pentose utilization in Saccharomyces cerevisiae. Adv. Biochem. Eng. Biotechnol. 2007, 108:147-177.
11. Han M.J., Lee J.W., Lee S.Y. Understanding and engineering of microbial cells based on proteomics and its conjunction with other omics studies. Proteomics. 2011, 11:721-743.
12. Hasunuma T., Ismail K.S., Nambu Y., Kondo A. Co-expression of TAL1 and ADH1 in recombinant xylose-fermenting Saccharomyces cerevisiae improves ethanol production from lignocellulosic hydrolysates in the presence of furfural. J. Biosci. Bioeng. 2014, 117:165-169.
13. Ho N.W.Y., Chen Z., Brainard A.P. Genetically engineered Saccharomyces yeast capable of effective co-fermentation of glucose and xylose. Appl. Env. Microbiol. 1998, 64:1852-1859.
14. Jakociunas T., Bonde I., Herrgard M., Harrison S.J., Kristensen M., Pedersen L.E., Jensen M.K., Keasling J.D. Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae. Metab. Eng. 2015, 28:213-222.
15. Jin Y.-S., Alper H., Yang Y.-T., Stephanopoulos G. Improvement of xylose uptake and ethanol production in recombinant Saccharomyces cerevisiae through an inverse metabolic engineering approach. Appl. Environ. Microbiol. 2005, 71:8249-8256.
16. Jeffries T.W., Jin Y.S. Metabolic engineering for improved fermentation of pentoses by yeasts. Appl. Microbiol. Biotechnol. 2004, 63:495-509.
17. Kaneko Y., Tohe A., Banno I., Oshima Y. Molecular characterization of a specific para-nitrophenylphosphatase gene, Pho13, and its mapping by chromosome fragmentation in Saccharomyces cerevisiae. Mol. Gen. Genet. 1989, 220:133-139.
18. Karhumaa K., Fromanger R., Hahn-Hagerdal B., Gorwa-Grauslund M.F. High activity of xylose reductase and xylitol dehydrogenase improves xylose fermentation by recombinant Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 2007, 73:1039-1046.
19. Karhumaa K., Garcia Sanchez R., Hahn-Hagerdal B., Gorwa-Grauslund M.F. Comparison of the xylose reductase-xylitol dehydrogenase and the xylose isomerase pathways for xylose fermentation by recombinant Saccharomyces cerevisiae. Microb. Cell. Fact. 2007, 6:5.
20. Kim S., do Lee, Wohlgemuth Y., Park G., Fiehn H.S., Kim, K.H.O. Evaluation and optimization of metabolome sample preparation methods for Saccharomyces cerevisiae. Anal. Chem. 2013, 85:2169-2176.
21. Kim S.R., Park Y.C., Jin Y.S., Seo J.H. Strain engineering of Saccharomyces cerevisiae for enhanced xylose metabolism. Biotechnol. Adv. 2013, 31:851-861.
22. Kim S.R., Skerker J.M., Kang W., Lesmana A., Wei N., Arkin A.P., Jin Y.S. Rational and evolutionary engineering approaches uncover a small set of genetic changes efficient for rapid xylose fermentation in Saccharomyces cerevisiae. Plos One 2013, 8:e57048.
23. Kim S.R., Xu H., Lesmana A., Kuzmanovic U., Au M., Florencia C., Oh E.J., Zhang G., Kim K.H., Jin Y.-S. Deletion of PHO13 encoding HAD type IIA phosphatase results in upregulation of the pentose phosphate pathway in yeast. Appl. Env. Microbiol. 2015, 81:1601-1609.
24. Kuyper M., Hartog M.M., Toirkens M.J., Almering M.J., Winkler A.A., van Dijken J.P., Pronk J.T. Metabolic engineering of a xylose-isomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation. Fems Yeast Res. 2005, 5:399-409.
25. Kuyper M., Toirkens M.J., Diderich J.A., Winkler A.A., van Dijken J.P., Pronk J.T. Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain. Fems Yeast Res. 2005, 5:925-934.
26. Latimer L.N., Lee M.E., Medina-Cleghorn D., Kohnz R.A., Nomura D.K., Dueber J.E. Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae. Metab. Eng. 2014, 25:20-29.
27. Lee do Y., Fiehn O. High quality metabolomic data for Chlamydomonas reinhardtii. Plant Methods 2008, 4:7.
28. Lee S.H., Kim S., Kwon M.A., Jung Y.H., Shin Y.A., Kim K.H. Atmospheric vs. anaerobic processing of metabolome samples for the metabolite profiling of a strict anaerobic bacterium, Clostridium acetobutylicum. Biotechnol. Bioeng. 2014, 111:2528-2536.
29. Lee S.M., Jellison T., Alper H.S. Systematic and evolutionary engineering of a xylose isomerase-based pathway in Saccharomyces cerevisiae for efficient conversion yields. Biotechnol. Biofuels 2014, 7.
30. Li Y.C., Gou Z.X., Liu Z.S., Tang Y.Q., Akamatsu T., Kida K. Synergistic effects of TAL1 over-expression and PHO13 deletion on the weak acid inhibition of xylose fermentation by industrial Saccharomyces cerevisiae strain. Biotechnol. Lett. 2014, 36:2011-2021.
31. Liu E.K., Hu Y. Construction of a xylose-fermenting Saccharomyces cerevisiae strain by combined approaches of genetic engineering, chemical mutagenesis and evolutionary adaptation. Biochem. Eng. J. 2010, 48:204-210.
32. Lu C., Jeffries T. Shuffling of promoters for multiple genes to optimize xylose fermentation in an engineered Saccharomyces cerevisiae strain. Appl. Environ. Microbiol. 2007, 73:6072-6077.
33. Mans R., van Rossum H.M., Wijsman M., Backx A., Kuijpers N.G., van den Broek M., Daran-Lapujade P., Pronk J.T., van Maris A.J., Daran J.M. CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. Fems Yeast Res. 2015, 15.
34. Matsushika A., Goshima T., Fujii T., Inoue H., Sawayama S., Yano S. Characterization of non-oxidative transaldolase and transketolase enzymes in the pentose phosphate pathway with regard to xylose utilization by recombinant Saccharomyces cerevisiae. Enzym. Microb. Technol. 2012, 51:16-25.
35. Matsushika A., Inoue H., Kodaki T., Sawayama S. Ethanol production from xylose in engineered Saccharomyces cerevisiae strains: current state and perspectives. Appl. Microbiol. Biotechnol. 2009, 84:37-53.
36. Matsushika A., Nagashima A., Goshima T., Hoshino T. Fermentation of xylose causes inefficient metabolic state due to carbon/energy starvation and reduced glycolytic flux in recombinant industrial Saccharomyces cerevisiae. Plos One 2013, 8:e69005.
37. Ni H., Laplaza J.M., Jeffries T.W. Transposon mutagenesis to improve the growth of recombinant Saccharomyces cerevisiae on D-xylose. Appl. Environ. Microbiol. 2007, 73:2061-2066.
38. Olsson L., Nielsen J. The role of metabolic engineering in the improvement of Saccharomyces cerevisiae: utilization of industrial media. Enzym. Microb. Technol. 2000, 26:785-792.
39. Park N.H., Yoshida S., Takakashi A., Kawabata Y., Sun H.J., Kusakabe I. A new method for the preparation of crystalline L-arabinose from arabinoxylan by enzymatic hydrolysis and selective fermentation with yeast. Biotechnol. Lett. 2001, 23:411-416.
40. Park S.J., Lee S.Y., Cho J., Kim T.Y., Lee J.W., Park J.H., Han M.J. Global physiological understanding and metabolic engineering of microorganisms based on omics studies. Appl. Microbiol. Biotechnol. 2005, 68:567-579.
41. Peng B.Y., Huang S.C., Liu T.T., Geng A.L. Bacterial xylose isomerases from the mammal gut Bacteroidetes cluster function in Saccharomyces cerevisiae for effective xylose fermentation. Microb. Cell. Fact. 2015, 14.
42. Peng B.Y., Shen Y., Li X.W., Chen X., Hou J., Bao X.M. Improvement of xylose fermentation in respiratory-deficient xylose-fermenting Saccharomyces cerevisiae. Metab. Eng. 2012, 14:9-18.
43. Runquist D., Hahn-Hagerdal B., Bettiga M. Increased ethanol productivity in xylose-utilizing Saccharomyces cerevisiae via a randomly mutagenized xylose reductase. Appl. Environ. Microbiol. 2010, 76:7796-7802.
44. Ryan O.W., Cate J.H. Multiplex engineering of industrial yeast genomes using CRISPRm. Methods Enzym. 2014, 546:473-489.
45. Saeed A.I., Bhagabati N.K., Braisted J.C., Liang W., Sharov V., Howe E.A., Li J., Thiagarajan M., White J.A., Quackenbush J. TM4 microarray software suite. Methods Enzym. 2006, 411:134-193.
46. Sakihama Y., Hasunuma T., Kondo A. Improved ethanol production from xylose in the presence of acetic acid by the overexpression of the HAA1 gene in Saccharomyces cerevisiae. J. Biosci. Bioeng. 2015, 119:297-302.
47. Sanchez R.G., Karhumaa K., Fonseca C., Nogue V.S., Almeida J.R.M., Larsson C.U., Bengtsson O., Bettiga M., Hahn-Hagerdal B., Gorwa-Grauslund M.F. Improved xylose and arabinose utilization by an industrial recombinant Saccharomyces cerevisiae strain using evolutionary engineering. Biotechnol. Biofuels 2010, 3.
48. Senac T., Hahn-Hagerdal B. Intermediary metabolite concentrations in xylulose and glucose fermenting Saccharomyces cerevisiae cells. Appl. Environ. Microbiol. 1990, 56:120-126.
49. Sonderegger M., Sauer U. Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl. Environ. Microbiol. 2003, 69:1990-1998.
50. Takuma S., Nakashima N., Tantirungkij M., Kinoshita S., Okada H., Seki T., Yoshida T. Isolation of xylose reductase gene of Pichia stipitis and its expression in Saccharomyces cerevisiae. Appl. Biochem. Biotechnol. 1991, 28-9:327-340.
51. Tantirungkij M., Nakashima N., Seki T., Yoshida T. Construction of xylose assimilating Saccharomyces cerevisiae. J. Ferment. Bioeng. 1993, 75:83-88.
52. Tomitaka M., Taguchi H., Fukuda K., Akamatsu T., Kida K. Isolation and characterization of a mutant recombinant Saccharomyces cerevisiae strain with high efficiency xylose utilization. J. Biosci. Bioeng. 2013, 116:706-715.
53. Tuleva B., Vasileva-Tonkova E., Galabova D. A specific alkaline phosphatase from Saccharomyces cerevisiae with protein phosphatase activity. FEMS Microbiol. Lett. 1998, 161:139-144.
54. Ulrich E.L., Akutsu H., Doreleijers J.F., Harano Y., Ioannidis Y.E., Lin J., Livny M., Mading S., Maziuk D., Miller Z., Nakatani E., Schulte C.F., Tolmie D.E., Wenger R.K., Yao H.Y., Markley J.L. BioMagResBank. Nucleic Acids Res. 2008, 36:D402-D408.
55. Van Vleet J.H., Jeffries T.W., Olsson L. Deleting the para-nitrophenyl phosphatase (pNPPase), PHO13, in recombinant Saccharomyces cerevisiae improves growth and ethanol production on D-xylose. Metab. Eng. 2008, 10:360-369.
56. Vemuri G.N., Aristidou A.A. Metabolic engineering in the -omics era: Elucidating and modulating regulatory networks. Microbiol. Mol. Biol. R. 2005, 69:197.
57. Walfridsson M., Hallborn J., Penttila M., Keranen S., Hahn-Hagerdal B. Xylose-metabolizing Saccharomyces cerevisiae strains overexpressing the TKL1 and TAL1 genes encoding the pentose phosphate pathway enzymes transketolase and transaldolase. Appl. Environ. Microbiol. 1995, 61:4184-4190.
58. Wisselink H.W., Toirkens M.J., Wu Q., Pronk J.T., van Maris A.J.A. Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl. Environ. Microbiol. 2009, 75:907-914.
59. Zhang G.C., Kong I.I., Kim H., Liu J.J., Cate J.H., Jin Y.S. Construction of a quadruple auxotrophic mutant of an industrial polyploid Saccharomyces cerevisiae strain by using RNA-guided Cas9 nuclease. Appl. Environ. Microbiol. 2014, 80:7694-7701.
60. Zhou H., Cheng J.S., Wang B.L., Fink G.R., Stephanopoulos G. Xylose isomerase overexpression along with engineering of the pentose phosphate pathway and evolutionary engineering enable rapid xylose utilization and ethanol production by Saccharomyces cerevisiae. Metab. Eng. 2012, 14:611-622.