In vivo continuous evolution of genes and pathways in yeast

Nature Communications

Volumn 7, Issue , 2016, Pages

  Crook, Nathan ^a   Abatemarco, Joseph ^a   Sun, Jie ^a   Wagner, James M ^a   Schmitz, Alexander ^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

[No Author keywords available]

Indexed keywords

ENZYME;

CYTOGENETICS; ENZYME; EUKARYOTE; EVOLUTIONARY BIOLOGY; GENE; GENETIC ENGINEERING; GROWTH; MUTATION; YEAST;

ARTICLE; CONTROLLED STUDY; EVOLUTION; FUNGAL GENE; FUNGAL STRAIN; FUNGUS MUTANT; IN VIVO CONTINUOUS EVOLUTION; IN VIVO STUDY; KLUYVEROMYCES LACTIS; NONHUMAN; RETROPOSON; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; YEAST; BIOLOGICAL MODEL; CLASSIFICATION; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; KLUYVEROMYCES; METABOLISM; MUTATION; PROCEDURES;

EUKARYOTA; KLUYVEROMYCES LACTIS;

DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION REGULATION, FUNGAL; GENE LIBRARY; GENES, FUNGAL; KLUYVEROMYCES; METABOLIC NETWORKS AND PATHWAYS; MODELS, GENETIC; MUTAGENESIS, INSERTIONAL; MUTATION; RETROELEMENTS; SACCHAROMYCES CEREVISIAE; YEASTS;

EID: 84992075174     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms13051     Document Type: Article

References (63)

1. Chen, K., Arnold, F. H. Tuning the activity of an enzyme for unusual environments: sequential random mutagenesis of subtilisin E for catalysis in dimethylformamide. Proc. Natl Acad. Sci. USA 90, 5618-5622 (1993).
2. Stemmer, W. P. Rapid evolution of a protein in vitro by DNA shuffling. Nature 370, 389-391 (1994).
3. Jiang, L. et al. De novo computational design of retro-aldol enzymes. Science 319, 1387-1391 (2008).
4. Rothlisberger, D. et al. Kemp elimination catalysts by computational enzyme design. Nature 453, 190-195 (2008).
5. Zastrow, M. L., PeacockAnna, F. A., Stuckey, J. A., Pecoraro, V. L. Hydrolytic catalysis and structural stabilization in a designed metalloprotein. Nat. Chem. 4, 118-123 (2012).
6. Alper, H., Moxley, J., Nevoigt, E., Fink, G. R., Stephanopoulos, G. Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314, 1565-1568 (2006).
7. Brustad, E. M. et al. Structure-guided directed evolution of highly selective p450-based magnetic resonance imaging sensors for dopamine and serotonin. J. Mol. Biol. 422, 245-262 (2012).
8. Chen, Z., Zhao, H. Rapid creation of a novel protein function by in vitro coevolution. J. Mol. Biol. 348, 1273-1282 (2005).
9. Cho, G. S., Szostak, J. W. Directed evolution of ATP binding proteins from a zinc finger domain by using mRNA display. Chem. Biol. 13, 139-147 (2006).
10. Fasan, R., Meharenna, Y. T., Snow, C. D., Poulos, T. L., Arnold, F. H. Evolutionary history of a specialized p450 propane monooxygenase. J. Mol. Biol. 383, 1069-1080 (2008).
11. Dickinson, B. C., Leconte, A. M., Allen, B., Esvelt, K. M., Liu, D. R. Experimental interrogation of the path dependence and stochasticity of protein evolution using phage-assisted continuous evolution. Proc. Natl Acad. Sci. USA 110, 9007-9012 (2013).
12. Romero, P. A., Tran, T. M., Abate, A. R. Dissecting enzyme function with microfluidic-based deep mutational scanning. Proc. Natl Acad. Sci. USA 112, 7159-7164 (2015).
13. Esvelt, K. M., Carlson, J. C., Liu, D. R. A system for the continuous directed evolution of biomolecules. Nature 472, 499-U550 (2011).
14. Dickinson, B. C., Packer, M. S., Badran, A. H., Liu, D. R. A system for the continuous directed evolution of proteases rapidly reveals drug-resistance mutations. Nat. Commun. 5, 5352 (2014).
15. Carlson, J. C., Badran, A. H., Guggiana-Nilo, D. A., Liu, D. R. Negative selection and stringency modulation in phage-assisted continuous evolution. Nat. Chem. Biol. 10, 216-222 (2014).
16. Badran, A. H. et al. Continuous evolution of Bacillus thuringiensis toxins overcomes insect resistance. Nature 533, 58-63 (2016).
17. Wang, H. H. et al. Programming cells by multiplex genome engineering and accelerated evolution. Nature 460, 894-U133 (2009).
18. DiCarlo, J. E. et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 41, 4336-4343 (2013).
19. Findlay, G. M., Boyle, E. A., Hause, R. J., Klein, J. C., Shendure, J. Saturation editing of genomic regions by multiplex homology-directed repair. Nature 513, 120-123 (2014).
20. Ravikumar, A., Arrieta, A., Liu, C. C. An orthogonal DNA replication system in yeast. Nat. Chem. Biol. 10, 175-177 (2014).
21. Romanini, D. W., Peralta-Yahya, P., Mondol, V., Cornish, V. W. A heritable recombination system for synthetic Darwinian evolution in yeast. ACS Synth. Biol. 1, 602-609 (2012).
22. Wilhelm, F. X., Wilhelm, M., Gabriel, A. Reverse transcriptase and integrase of the Saccharomyces cerevisiae Ty1 element. Cytogenet. Genome Res. 110, 269-287 (2005).
23. Boeke, J. D., Xu, H., Fink, G. R. A general method for the chromosomal amplification of genes in yeast. Science 239, 280-282 (1988).
24. Curcio, M. J., Garfinkel, D. J. Single-step selection for Ty1 element retrotransposition. Proc. Natl Acad. Sci. USA 88, 936-940 (1991).
25. Gabriel, A., Willems, M., Mules, E. H., Boeke, J. D. Replication infidelity during a single cycle of Ty1 retrotransposition. Proc. Natl Acad. Sci. USA 93, 7767-7771 (1996).
26. Boutabout, M., Wilhelm, M., Wilhelm, F.-X. DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Ty1. Nucleic Acids Res. 29, 2217-2222 (2001).
27. Smith, J. S., Boeke, J. D. An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 11, 241-254 (1997).
28. Holstege, F. C. et al. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728 (1998).
29. Scholes, D. T., Banerjee, M., Bowen, B., Curcio, M. J. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159, 1449-1465 (2001).
30. Chan, J. E., Kolodner, R. D. A genetic and structural study of genome rearrangements mediated by high copy repeat Ty1 elements. PLoS Genet. 7, e1002089 (2011).
31. Qian, Z. et al. Yeast Ty1 retrotransposition is stimulated by a synergistic interaction between mutations in chromatin assembly factor I and histone regulatory proteins. Mol. Cell Biol. 18, 4783-4792 (1998).
32. Luria, S. E., Delbrück, M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28, 491-511 (1943).
33. Paquin, C. E., Williamson, V. M. Temperature effects on the rate of ty transposition. Science 226, 53-55 (1984).
34. Curran, K. A. et al. Short synthetic terminators for improved heterologous gene expression in yeast. ACS Synth. Biol. 4, 824-832 (2015).
35. Beekwilder, J. et al. Polycistronic expression of a beta-carotene biosynthetic pathway in Saccharomyces cerevisiae coupled to beta-ionone production. J. Biotechnol. 192(Pt B): 383-392 (2014).
36. Cormack, B. P., Struhl, K. The TATA-binding protein is required for transcription by all three nuclear RNA polymerases in yeast cells. Cell 69, 685-696 (1992).
37. Young, E., Poucher, A., Comer, A., Bailey, A., Alper, H. Functional survey for heterologous sugar transport proteins, using Saccharomyces cerevisiae as a host. Appl. Environ. Microbiol. 77, 3311-3319 (2011).
38. 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. 78, 5708-5716 (2012).
39. Träff, K. L., Otero Cordero, R. R., van Zyl, W. H., Hahn-Hägerdal, B. Deletion of the GRE3 aldose reductase gene and its influence on xylose metabolism in recombinant strains of Saccharomyces cerevisiae expressing thexylA and XKS1 genes. Appl. Environ. Microbiol. 67, 5668-5674 (2001).
40. Blazeck, J., Garg, R., Reed, B., Alper, H. S. Controlling promoter strength and regulation in Saccharomyces cerevisiae using synthetic hybrid promoters. Biotechnol. Bioeng. 109, 2884-2895 (2012).
41. Eriksen, D. T., Hsieh, P. C., Lynn, P., Zhao, H. Directed evolution of a cellobiose utilization pathway in Saccharomyces cerevisiae by simultaneously engineering multiple proteins. Microb. Cell Fact 12, 61 (2013).
42. Lee, W.-K. Cloned Gene Integration in Recombinant Yeast and Application to Metabolic Engineering (Univ. California Irvine, 2003).
43. Sambrook, J., Russell, D. W. Molecular Cloning: a Laboratory Manual 3rd edn (Cold Spring Harbor Laboratory, 2001).
44. Hegemann, J. H., Heick, S. B. Delete and repeat: a comprehensive toolkit for sequential gene knockout in the budding yeast Saccharomyces cerevisiae. Methods Mol. Biol. 765, 189-206 (2011).
45. Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).
46. Guldener, U., Heck, S., Fielder, T., Beinhauer, J., Hegemann, J. H. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24, 2519-2524 (1996).
47. Lamprecht, M. R., Sabatini, D. M., Carpenter, A. E. CellProfiler(TM): free, versatile software for automated biological image analysis. BioTechniques 42, 71-75 (2007).
48. Hall, B. M., Ma, C. X., Liang, P., Singh, K. K. Fluctuation AnaLysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25, 1564-1565 (2009).
49. Ma, W. T., Sandri, G. V., Sarkar, S. Analysis of the Luria-Delbrück distribution using discrete convolution powers. J. Appl. Probab. 29, 255-267 (1992).
50. Lamprecht, M. R., Sabatini, D. M., Carpenter, A. E. CellProfiler: free, versatile software for automated biological image analysis. BioTechniques 42, 71-75 (2007).
51. Masella, A. P., Bartram, A. K., Truszkowski, J. M., Brown, D. G., Neufeld, J. D. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics 13, 31 (2012).
52. Najoshi, https://github. com/najoshi/sabre. git.
53. Patel, R. K., Jain, M. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7, e30619 (2012).
54. Ning, Z., Cox, A. J., Mullikin, J. C. SSAHA: a fast search method for large DNA databases. Genome Res. 11, 1725-1729 (2001).
55. Clopper, C. J., Pearson, E. S. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 26, 404-413 (1934).
56. Moriya, H., Shimizu-Yoshida, Y., Kitano, H. In vivo robustness analysis of cell division cycle genes in Saccharomyces cerevisiae. PLoS Genet. 2, e111 (2006).
57. Kersters-Hilderson, H., Callens, M., Van Opstal, O., Vangrysperre, W., De Bruyne, C. K. Kinetic characterization of d-xylose isomerases by enzymatic assays using d-sorbitol dehydrogenase. Enzyme Microb. Technol. 9, 145-148 (1987).
58. Schwede, T., Kopp, J., Guex, N., Peitsch, M. C. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385 (2003).
59. Ren, P. Y., Ponder, J. W. Polarizable atomic multipole water model for molecular mechanics simulation. J. Phys. Chem. B 107, 5933-5947 (2003).
60. Schneidman-Duhovny, D., Inbar, Y., Nussinov, R., Wolfson, H. J. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 33, W363-W367 (2005).
61. Tovchigrechko, A., Vakser, I. A. GRAMM-X public web server for protein-protein docking. Nucleic Acids Res. 34, W310-W314 (2006).
62. Schrodinger, L. L. C. The PyMOL Molecular Graphics System, Version 1. 3r1 (2010).
63. Zhu, Y. O., Siegal, M. L., Hall, D. W., Petrov, D. A. Precise estimates of mutation rate and spectrum in yeast. Proc. Natl Acad. Sci. USA 111, E2310-E2318 (2014).