Expanding the metabolic engineering toolbox with directed evolution

Biotechnology Journal

Volumn 8, Issue 12, 2013, Pages 1397-1410

  Abatemarco, Joseph ^a   Hill, Andrew ^a   Alper, Hal S ^a,b  

^a The University of Texas at Austin   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Directed evolution; Metabolic engineering; Pathway engineering; Synthetic biology

Indexed keywords

DIRECTED EVOLUTION; GENE OVER-EXPRESSION; HIGH-VALUE CHEMICALS; METABOLIC PATHWAY ENGINEERING; PATHWAY ENGINEERINGS; RENEWABLE FEEDSTOCKS; SYNTHETIC BIOLOGY; TRADITIONAL APPROACHES;

METABOLISM;

METABOLIC ENGINEERING;

ENZYME; GLUCOSE TRANSPORTER;

BINDING AFFINITY; CATALYST; CELL METABOLISM; DIRECTED MOLECULAR EVOLUTION; GENE DELETION; GENE OVEREXPRESSION; GENETIC SCREENING; GENOME; METABOLIC ENGINEERING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ENGINEERING; REGULATORY MECHANISM; REVIEW;

DIRECTED EVOLUTION; METABOLIC ENGINEERING; PATHWAY ENGINEERING; SYNTHETIC BIOLOGY;

DIRECTED MOLECULAR EVOLUTION; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; SYSTEMS BIOLOGY;

EID: 84889671228     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201300021     Document Type: Review

References (81)

1. Jang, Y.-S., Lee, J. Y., Lee, J., Park, J. H. et al., Enhanced butanol production obtained by reinforcing the direct butanol-forming route in Clostridium acetobutylicum. mBio 2012, 3, e00314-00312.
2. Steen, E., Chan, R., Prasad, N., Myers, S. et al., Metabolic engineering of Saccharomyces cerevisiae for the production of n-butanol. Microb. Cell Fact. 2008, 7, 36.
3. Hong, S. H., Lee, S. Y., Metabolic flux analysis for succinic acid production by recombinant Escherichia coli with amplified malic enzyme activity. Biotechnol. Bioeng. 2001, 74, 89-95.
4. Curran, K. A., Leavitt, J. M., Karim, A. S., Alper, H. S., Metabolic engineering of muconic acid production in Saccharomyces cerevisiae. Metab. Eng. 2013, 15, 55-66.
5. Schirmer, A., Rude, M. A., Li, X., Popova, E. et al., Microbial biosynthesis of alkanes. Science 2010, 329, 559-562.
6. Curran, K. A., Alper, H. S., Expanding the chemical palate of cells by combining systems biology and metabolic engineering. Metab. Eng. 2012, 14, 289-297.
7. Pourmir, A., Johannes, T., Directed evolution: Selection of the host organism. Comput. Struct. Biotechnol. J. 2012, 2. e201209012.
8. Liu, L., Redden, H., Alper, H. S., Frontiers of yeast metabolic engineering: diversifying beyond ethanol and Saccharomyces. Curr. Opin. Biotechnol. 2013, DOI: 10.1016/j.copbio.2013.03.005. [Epub ahead of print].
9. Lanza, A. M., Crook, N. C., Alper, H. S., Innovation at the intersection of synthetic and systems biology. Curr. Opin. Biotechnol. 2012, 23, 712-717.
10. Blazeck, J., Alper, H., Systems metabolic engineering: Genome-scale models and beyond. Biotechnol. J. 2010, 5, 647-659.
11. Lee, J. W., Na, D., Park, J. M., Lee, J. et al., Systems metabolic engineering of microorganisms for natural and non-natural chemicals. Nat. Chem. Biol. 2012, 8, 536-546.
12. Arnold, F. H., Design by directed evolution. Acc. Chem. Res. 1998, 31, 125-131.
13. Voigt, C. A., Martinez, C., Wang, Z.-G., Mayo, S. L. et al., Protein building blocks preserved by recombination. Nat. Struct. Mol. Biol. 2002, 9, 553-558.
14. Chen, F., Gaucher, E. A., Leal, N. A., Hutter, D. et al., Reconstructed evolutionary adaptive paths give polymerases accepting reversible terminators for sequencing and SNP detection. Proc. Natl. Acad. Sci. USA 2010, 107, 1948-1953.
15. Yamashiro, K., Yokobori, S.-I., Koikeda, S., Yamagishi, A., Improvement of Bacillus circulans β-amylase activity attained using the ancestral mutation method. Protein Eng. Des. Sel. 2010, 23, 519-528.
16. Farinas, E. T., Schwaneberg, U., Glieder, A., Arnold, F. H., Directed evolution of a cytochrome P450 monooxygenase for alkane oxidation. Adv. Synth. Catal. 2001, 343, 601-606.
17. Lee, S.-M., Jellison, T., Alper, H. S., Directed evolution of xylose isomerase for improved xylose catabolism and fermentation in the yeast Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2012, 78, 5708-5716.
18. Young, E. M., Comer, A. D., Huang, H., Alper, H. S., A molecular transporter engineering approach to improving xylose catabolism in Saccharomyces cerevisiae. Metab. Eng. 2012, 14, 401-411.
19. Romero, P. A., Arnold, F. H., Exploring protein fitness landscapes by directed evolution. Nat. Rev. Mol. Cell Biol. 2009, 10, 866-876.
20. Hibbert, E. G., Baganz, F., Hailes, H. C., Ward, J. M. et al., Directed evolution of biocatalytic processes. Biomol. Eng. 2005, 22, 11-19.
21. Wang, C.-w., Oh, M.-K., Liao, J. C., Directed evolution of metabolically engineered Escherichia coli for carotenoid production. Biotechnol. Prog. 2000, 16, 922-926.
22. Sun, L., Bulter, T., Alcalde, M., Petrounia, I. P. et al., Modification of galactose oxidase to introduce glucose 6-oxidase activity. ChemBioChem 2002, 3, 781-783.
23. Koryakina, I., McArthur, J., Randall, S., Draelos, M. M. et al., Poly Specific trans-acyltransferase machinery revealed via engineered Acyl-CoA synthetases. ACS Chem. Biol. 2012, 8, 200-208.
24. Bastian, S., Liu, X., Meyerowitz, J. T., Snow, C. D. et al., Engineered ketol-acid reductoisomerase and alcohol dehydrogenase enable anaerobic 2-methylpropan-1-ol production at theoretical yield in Escherichia coli. Metab. Eng. 2011, 13, 345-352.
25. Joo, H., Lin, Z., Arnold, F. H., Laboratory evolution of peroxide-mediated cytochrome P450 hydroxylation. Nature 1999, 399, 670-673.
26. Sun, L., Petrounia, I. P., Yagasaki, M., Bandara, G. et al., Expression and stabilization of galactose oxidase in Escherichia coli by directed evolution. Protein Eng. 2001, 14, 699-704.
27. Alper, H., Moxley, J., Nevoigt, E., Fink, G. R. et al., Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 2006, 314, 1565-1568.
28. Tang, S.-Y., Fazelinia, H., Cirino, P. C., AraC regulatory protein mutants with altered effector specificity. J. Am. Chem. Soc. 2008, 130, 5267-5271.
29. Boder, E. T., Wittrup, K. D., Yeast surface display for screening combinatorial polypeptide libraries. Nat. Biotechnol. 1997, 15, 553-557.
30. Crameri, A., Dawes, G., Rodriguez Jr, E., Silver, S. et al., Molecular evolution of an arsenate detoxification pathway by DNA shuffling. Nat. Biotechnol. 1997, 15, 436-438.
31. Patnaik, R., Louie, S., Gavrilovic, V., Perry, K. et al., Genome shuffling of Lactobacillus for improved acid tolerance. Nat. Biotechnol. 2002, 20, 707-712.
32. Otte, B., Grunwaldt, E., Mahmoud, O., Jennewein, S., Genome shuffling in Clostridium diolis DSM 15410 for improved 1, 3-propanediol production. Appl. Environ. Microbiol. 2009, 75, 7610-7616.
33. Winkler, J., Kao, K. C., Harnessing recombination to speed adaptive evolution in Escherichia coli. Metab. Eng. 2012, 14, 487-495.
34. Portnoy, V. A., Bezdan, D., Zengler, K., Adaptive laboratory evolution - harnessing the power of biology for metabolic engineering. Curr. Opin. Biotechnol. 2011, 22, 590-594.
35. Fox, R. J., Clay, M. D., Catalytic effectiveness, a measure of enzyme proficiency for industrial applications. Trends Biotechnol. 2009, 27, 137-140.
36. Coelho, P. S., Brustad, E. M., Kannan, A., Arnold, F. H., Olefin cyclopropanation via carbene transfer catalyzed by engineered cytochrome P450 enzymes. Science 2013, 339, 307-310.
37. Ben-David, M., Wieczorek, G., Elias, M., Silman, I. et al., Catalytic metal ion rearrangements underline promiscuity and evolvability of a metalloenzyme. J. Mol. Biol. 2013, 425, 1028-1038.
38. Suzuki, Y., Asada, K., Miyazaki, J., Tomita, T. et al., Enhancement of the latent 3-isopropylmalate dehydrogenase activity of promiscuous homoisocitrate dehydrogenase by directed evolution. Biochem. J. 2010, 431, 401-410.
39. Umeno, D., Arnold, F. H., Evolution of a pathway to novel long-chain carotenoids. J. Bacteriol. 2004, 186, 1531-1536.
40. Tobias, A. V., Arnold, F. H., Biosynthesis of novel carotenoid families based on unnatural carbon backbones: A model for diversification of natural product pathways. Biochim. Biophys. Acta 2006, 1761, 235-246.
41. Yoshikuni, Y., Ferrin, T. E., Keasling, J. D., Designed divergent evolution of enzyme function. Nature 2006, 440, 1078-1082.
42. Ji, X.-J., Xia, Z.-F., Fu, N.-H., Nie, Z.-K. et al., Cofactor engineering through heterologous expression of an NADH oxidase and its impact on metabolic flux redistribution in Klebsiella pneumoniae. Biotechnol. Biofuels 2013, 6, 7.
43. Hasegawa, S., Suda, M., Uematsu, K., Natsuma, Y. et al., Engineering of Corynebacterium glutamicum for high yield L-valine production under oxygen deprivation conditions. Appl. Environ. Microbiol. 2013, 79, 1250-1257.
44. Alberstein, M., Eisenstein, M., Abeliovich, H., Removing allosteric feedback inhibition of tomato 4-coumarate:CoA ligase by directed evolution. Plant J. 2012, 69, 57-69.
45. Báez-Viveros, J. L., Osuna, J., Hernández-Chávez, G., Soberón, X. et al., Metabolic engineering and protein directed evolution increase the yield of L-phenylalanine synthesized from glucose in Escherichia coli. Biotechnol. Bioeng. 2004, 87, 516-524.
46. Atsumi, S., Liao, J. C., Directed evolution of Methanococcus jannaschii citramalate synthase for biosynthesis of 1-propanol and 1-butanol by Escherichia coli. Appl. Environ. Microbiol. 2008, 74, 7802-7808.
47. Alper, H., Fischer, C., Nevoigt, E., Stephanopoulos, G., Tuning genetic control through promoter engineering. Proc. Natl. Acad. Sci. USA 2005, 102, 12678-12683.
48. Blazeck, J., Alper, H. S., Promoter engineering: Recent advances in controlling transcription at the most fundamental level. Biotechnol. J. 2013, 8, 46-58.
49. Nevoigt, E., Kohnke, J., Fischer, C. R., Alper, H. et al., Engineering of promoter replacement cassettes for fine-tuning of gene expression in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2006, 72, 5266-5273.
50. Nevoigt, E., Fischer, C., Mucha, O., Matthäus, F. et al., Engineering promoter regulation. Biotechnol. Bioeng. 2007, 96, 550-558.
51. Kagiya, G., Ogawa, R., Hatashita, M., Takagi, K. et al., Generation of a strong promoter for Escherichia coli from eukaryotic genome DNA. J. Biotechnol. 2005, 115, 239-248.
52. Vee Aune, T. E., Bakke, I., Drabløs, F., Lale, R. et al., Directed evolution of the transcription factor XylS for development of improved expression systems. Microb. Biotechnol. 2010, 3, 38-47.
53. Lee, S. K., Chou, H. H., Pfleger, B. F., Newman, J. D. et al., Directed Evolution of AraC for Improved Compatibility of Arabinose- and Lactose-Inducible Promoters. Appl. Environ. Microbiol. 2007, 73, 5711-5715.
54. Koyanagi, T., Katayama, T., Suzuki, H., Onishi, A. et al., Hyperproduction of 3, 4-dihydroxyphenyl-L-alanine (L-dopa) using Erwinia herbicola cells carrying a mutant transcriptional regulator TyrR. Biosci. Biotechnol. Biochem. 2009, 73, 1221-1223.
55. Alper, H., Stephanopoulos, G., Global transcription machinery engineering: A new approach for improving cellular phenotype. Metab. Eng. 2007, 9, 258-267.
56. Klein-Marcuschamer, D., Santos, C. N. S., Yu, H., Stephanopoulos, G., Mutagenesis of the bacterial RNA polymerase alpha subunit for improvement of complex phenotypes. Appl. Environ. Microbiol. 2009, 75, 2705-2711.
57. Zhang, H., Chong, H., Ching, C. B., Jiang, R., Random mutagenesis of global transcription factor cAMP receptor protein for improved osmotolerance. Biotechnol. Bioeng. 2012, 109, 1165-1172.
58. Klein-Marcuschamer, D., Stephanopoulos, G., Assessing the potential of mutational strategies to elicit new phenotypes in industrial strains. Proc. Natl. Acad. Sci. USA 2008, 105, 2319-2324.
59. Xiong, A.-S., Jiang, H.-H., Zhuang, J., Peng, R.-H. et al., Expression and function of a modified AP2/ERF transcription factor from Brassica napus enhances cold tolerance in transgenic Arabidopsis. Mol. Biotechnol. 2013, 53, 198-206.
60. Farmer, W. R., Liao, J. C., Improving lycopene production in Escherichia coli by engineering metabolic control. Nat. Biotechnol. 2000, 18, 533-537.
61. Zhang, F., Keasling, J., Biosensors and their applications in microbial metabolic engineering. Trends Microbiol. 2011, 19, 323-329.
62. Reed, B., Blazeck, J., Alper, H., Evolution of an alkane-inducible biosensor for increased responsiveness to short-chain alkanes. J. Biotechnol. 2012, 158, 75-79.
63. Collins, C. H., Leadbetter, J. R., Arnold, F. H., Dual selection enhances the signaling specificity of a variant of the quorum-sensing transcriptional activator LuxR. Nat. Biotechnol. 2006, 24, 708-712.
64. Tang, S.-Y., Cirino, P. C., Design and application of a mevalonate-responsive regulatory protein. Angew. Chem. Int. Ed. Engl. 2011, 50, 1084-1086.
65. Bayer, T. S., Smolke, C. D., Programmable ligand-controlled riboregulators of eukaryotic gene expression. Nat. Biotechnol. 2005, 23, 337-343.
66. Beisel, C. L., Bayer, T. S., Hoff, K. G., Smolke, C. D., Model-guided design of ligand-regulated RNAi for programmable control of gene expression. Mol. Syst. Biol. 2008, 4, 224.
67. Win, M. N., Smolke, C. D., A modular and extensible RNA-based gene-regulatory platform for engineering cellular function. Proc. Natl. Acad. Sci. USA 2007, 104, 14283-14288.
68. 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.
69. Ren, C., Chen, T., Zhang, J., Liang, L. et al., An evolved xylose transporter from Zymomonas mobilis enhances sugar transport in Escherichia coli. Microb. Cell Fact. 2009, 8, 66.
70. Bokma, E., Koronakis, E., Lobedanz, S., Hughes, C. et al., Directed evolution of a bacterial efflux pump: Adaptation of the E. coli TolC exit duct to the Pseudomonas MexAB translocase. FEBS Lett. 2006, 580, 5339-5343.
71. Dunlop, M. J., Dossani, Z. Y., Szmidt, H. L., Chu, H. C. et al., Engineering microbial biofuel tolerance and export using efflux pumps. Mol. Syst. Biol. 2011, 7, 487.
72. Foo, J., Leong, S., Directed evolution of an E. coli inner membrane transporter for improved efflux of biofuel molecules. Biotechnol. Biofuels 2013, 6, 81.
73. Zhang, Y.-X., Perry, K., Vinci, V. A., Powell, K. et al., Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature 2002, 415, 644-646.
74. Conrad, T. M., Lewis, N. E., Palsson, B. O., Microbial laboratory evolution in the era of genome-scale science. Mol. Syst. Biol. 2011, 7, 509.
75. Conrad, T. M., Frazier, M., Joyce, A. R., Cho, B.-K. et al., RNA polymerase mutants found through adaptive evolution reprogram Escherichia coli for optimal growth in minimal media. Proc. Natl. Acad. Sci. USA 2010, 107, 20500-20505.
76. Zhang, X., Jantama, K., Moore, J. C., Jarboe, L. R. et al., Metabolic evolution of energy-conserving pathways for succinate production in Escherichia coli. Proc. Natl. Acad. Sci. USA 2009, 106, 20180-20185.
77. Unrean, P., Srienc, F., Metabolic networks evolve towards states of maximum entropy production. Metab. Eng. 2011, 13, 666-673.
78. Trinh, C. T., Srienc, F., Metabolic engineering of Escherichia coli for efficient conversion of glycerol to ethanol. Appl. Environ. Microbiol. 2009, 75, 6696-6705.
79. Fong, S. S., Burgard, A. P., Herring, C. D., Knight, E. M. et al., In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnol. Bioeng. 2005, 91, 643-648.
80. Esvelt, K. M., Carlson, J. C., Liu, D. R., A system for the continuous directed evolution of biomolecules. Nature 2011, 472, 499-503.
81. Agresti, J. J., Antipov, E., Abate, A. R., Ahn, K. et al., Ultrahigh-throughput screening in drop-based microfluidics for directed evolution. Proc. Natl. Acad. Sci. USA 2010, 107, 4004-4009.