Iterative optimization of xylose catabolism in Saccharomyces cerevisiae using combinatorial expression tuning

Biotechnology and Bioengineering

Volumn 114, Issue 6, 2017, Pages 1301-1309

  Latimer, Luke N ^a   Dueber, John E ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California at Berkeley   (United States)

Author keywords

combinatorial expression; metabolic engineering; synthetic biology; xylose utilization

Indexed keywords

ENZYMES; METABOLIC ENGINEERING; METABOLISM; YEAST;

COMBINATORIAL EXPRESSION; ENZYMATIC ACTIVITIES; FUNCTIONAL EXPRESSION; ITERATIVE OPTIMIZATION; MULTIPLE INTEGRATIONS; PRODUCTION IMPROVEMENT; SYNTHETIC BIOLOGY; XYLOSE UTILIZATIONS;

BIOCHEMICAL ENGINEERING;

XYLOSE; MULTIENZYME COMPLEX; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; COMBINATORIAL LIBRARY; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME DEGRADATION; FUNGAL BIOMASS; METABOLIC ENGINEERING; NONHUMAN; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; BIOLOGICAL MODEL; COMBINATORIAL CHEMISTRY; COMPUTER SIMULATION; GENETIC ENHANCEMENT; GENETICS; METABOLIC FLUX ANALYSIS; METABOLISM; PHYSIOLOGY; PROCEDURES;

COMBINATORIAL CHEMISTRY TECHNIQUES; COMPUTER SIMULATION; GENETIC ENHANCEMENT; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLISM; MODELS, BIOLOGICAL; MULTIENZYME COMPLEXES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; XYLOSE;

EID: 85013374260     PISSN: 00063592     EISSN: 10970290     Source Type: Journal    
DOI: 10.1002/bit.26262     Document Type: Article

References (40)

1. Ajikumar PK, Xiao WH, Tyo KEJ, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G. 2010. Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science 330:70–74.
2. Biggs BW, Paepe BD, Santos CNS, Mey MD, Ajikumar PK. 2014. Multivariate modular metabolic engineering for pathway and strain optimization. Curr Opin Biotechnol 29:156––62.
3. Brockman IM, Prather KLJ. 2015. Dynamic metabolic engineering: New strategies for developing responsive cell factories. Biotechnol J 10:1360–1369.
4. Chavez A, Tuttle M, Pruitt BW, Ewen-campen B, Chari R, Ter-ovanesyan D, Haque SJ, Cecchi RJ, Kowal EJK, Buchthal J, Housden BE, Perrimon N, Collins JJ, Church G. 2016. Comparison of Cas9 activators in multiple species. Nat Methods 13:563–569.
5. Chen S-H, Hwang D-R, Chen G-H, Hsu N-S, Wu Y-T, Li T-L, Wong C-H. 2012. Engineering transaldolase in Pichia stipitis to improve bioethanol production. ACS Chem Biol 7:481–486.
6. Chen R, Rishi HS, Potapov V, Yamada MR, Yeh VJ, Chow T, Cheung CL, Jones AT, Johnson TD, Keating AE, DeLoache WC, Dueber JE. 2015. A barcoding strategy enabling higher-throughput library screening by microscopy. ACS Synth Biol 4:1205–1216.
7. Chu BCH, Lee H. 2007. Genetic improvement of Saccharomyces cerevisiae for xylose fermentation. Biotechnol Adv 25:425–441.
8. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hus PD, Wu X, Jiang W, Marraffini LA, Zhang F. 2013. Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–822.
9. Deaner M, Alper HS. 2016. Promoter and terminator discovery and engineering. Adv Biochem Eng/Biotechnol 1–24.
10. Engler C, Marillonnet S. 2014. Golden gate cloning. Methods Mol Biol 1116:119–131.
11. Fell DA. 2005. Metabolic control analysis. Top Curr Genet 13:69–80.
12. Gietz RD, Woods RA. 2006. Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol Biol 313:107–120.
13. Guntas G, Purbeck C, Kuhlman B. 2010. Engineering a protein—protein interface using a computationally designed library. Proc Natl Acad Sci USA 107:19296–19301.
14. Hoynes-O'Connor A, Moon TS. 2015. Programmable genetic circuits for pathway engineering. Curr Opin Biotechnol 36:115–121.
15. Janczak M, Bukowski M, Goreck A, Dubin G, Dubin A, Wladyka B. 2015. A systematic investigation of the stability of green fluorescent protein fusion proteins. J Polish Biochem Soc 62:10–14.
16. Jensen NB, Strucko T, Kildegaard KR, David F, Maury J, Mortensen UH, Forster J, Nielsen J, Borodina I. 2014. Easyclone: Method for iterative chromosomal integration of multiple genes in Saccharomyces cerevisiae. FEMS Yeast Res 14:238–248.
17. Jin YS, Alper HS, Yang YT, Stephanopoulos G. 2005. Improvement of xylose uptake and ethanol production in recombinant Saccharomyces cerevisiae through an inverse metabolic engineering approach. Appl Environ Microbiol 71:8249.
18. Kafri M, Metzl-raz E, Jona G, Barkai N. 2016. The cost of protein production. Cell Rep 14:22–31.
19. Kaganovich D, Kopito R, Frydman J. 2008. Misfolded proteins partition between two distinct quality control compartments. Nature 454:1088–1096.
20. Kushwaha M, Salis HM. 2015. A portable expression resource for engineering cross-species genetic circuits and pathways. Nat Commun 6:1–11.
21. Latimer LN, Lee ME, Medina-Cleghorn D, Kohnz RA, Nomura DK, Dueber JE. 2014. Employing a combinatorial expression approach to characterize xylose utilization in Saccharomyces cerevisiae. Metab Eng 25:20–29.
22. Lee ME, Aswani A, Han AS, Tomlin CJ, Dueber JE. 2013. Expression-level optimization of a multi-enzyme pathway in the absence of a high-throughput assay. Nucleic Acids Res 1–11.
23. Lee ME, Deloache WC, Cervantes B, Dueber JE. 2015. A highly characterized yeast toolkit for modular, multipart assembly. ACS Synth Biol 4:975–986.
24. Leonard E, Ajikumar PK, Thayer K, Xiao W-H, Mo JD, Tidor B, Stephanopoulos G, Prather KLJ. 2010. Combining metabolic and protein engineering of a terpenoid biosynthetic pathway for overproduction and selectivity control. Proc Natl Acad Sci USA 107:13654–13659.
25. Lu C, Jeffries T. 2007. Shuffling of promoters for multiple genes to optimize xylose fermentation in an engineered Saccharomyces cerevisiae strain. Appl Environ Microbiol 73:6072–6077.
26. Matsushika A, Inoue H, Kodaki T, Sawayama S. 2009. Ethanol production from xylose in engineered Saccharomyces cerevisiae strains: current state and perspectives. Appl Microbiol Biotechnol 84:37–53.
27. Mutalik VK, Guimaraes JC, Cambray G, Lam C, Christoffersen MJ, Mai Q-A, Tran AB, Paull M, Keasling JD, Arkin AP, Endy D. 2013. Precise and reliable gene expression via standard transcription and translation initiation elements. Nat Genet 10:354–360.
28. Pandey RP, Parajuli P, Koffas MAG, Sohng JK. 2016. Microbial production of natural and non-natural flavonoids: Pathway engineering, directed evolution and systems/synthetic biology. Biotechnol Adv 34:634–662.
29. Redding-Johanson AM, Batth TS, Chan R, Krupa R, Szmidt HL, Adams PD, Keasling JD, Lee TS, Mukhopadhyay A, Petzold CJ. 2011. Targeted proteomics for metabolic pathway optimization: Application to terpene production. Metab Eng 13(2):194–203.
30. Ro D-K, Paradise EM, Ouellet M, Fisher KJ, Newman KL, Ndungu JM, Ho KA, Eachus RA, Ham TS, Kirby J, Chang MCY, Withers ST, Shiba Y, Sarpong R, Keasling JD. 2006. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440:3–6.
31. Romero PA, Krause A, Arnold FH. 2012. Navigating the protein fitness landscape with gaussian processes. Proc Natl Acad Sci USA 100:E193–E201.
32. Ryan OW, Skerker JM, Maurer MJ, Li X, Tsai JC, Poddar S, Lee ME, DeLoache WC, Dueber JE, Arkin AP, Cate JHD. 2014. Selection of chromosomal DNA libraries using a multiplex CRISPR system. Elife 3:1–15.
33. Santos CNS, Stephanopoulos G. 2008. Combinatorial engineering of microbes for optimizing cellular phenotype. Curr Opin Chem Biol 12:168–176.
34. Shi S, Liang Y, Zhang MM, Ang EL, Zhao H. 2016. A highly efficient single-step, markerless strategy for multi-copy chromosomal integration of large biochemical pathways in Saccharomyces cerevisiae. Metab Eng 33:19–27.
35. Stephanopoulos GN, Aristidou AA, Nielsen J. 1998. Metabolic engineering principles and methodologies. London: Elsevier Science. p 1–14.
36. Trenchard IJ, Smolke CD. 2015. Engineering strategies for the fermentative production of plant alkaloids in yeast. Metab Eng 30:96–104.
37. Voigt CA, Martinez C, Wang Z-G, May SL, Arnold FH. 2002. Protein building blocks preserved by recombination. Nat Struct Biol 9:553–558.
38. Wetmore KM, Price MN, Waters RJ, Lamson JS, He J, Hoover CA, Blow MJ, Bristow J, Butland G, Arkin AP, Deutschbauer A. 2015. Rapid quantification of mutant fitness in diverse bacteria by sequencing randomly bar-coded transposons. MBio 6:1–15.
39. Wingler LM, Cornish VW. 2011. Reiterative recombination for the in vivo assembly of libraries of multigene pathways. Proc Natl Acad Sci USA 108:15135–15140.
40. Yadav VG, Mey MD, Lim CG, Ajikumar PK, Stephanopoulos G. 2012. The future of metabolic engineering and synthetic biology: Towards a systematic practice. Metab Eng 14:233–241.