A population-based experimental model for protein evolution: Effects of mutation rate and selection stringency on evolutionary outcomes

Biochemistry

Volumn 52, Issue 8, 2013, Pages 1490-1499

  Leconte, Aaron M ^a   Dickinson, Bryan C ^a   Yang, David D ^a   Chen, Irene A ^b   Allen, Benjamin ^a,c   Liu, David R ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c EMMANUEL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRITICAL COMPONENT; EXPERIMENTAL MODELS; EXPERIMENTAL PLATFORM; HIGH-THROUGHPUT SEQUENCING; KEY DETERMINANTS; MUTATION RATES; POSITIVE SELECTION; PROTEIN EVOLUTION; PROTEIN SEQUENCES; RNA POLYMERASE; T7 RNA POLYMERASE;

PROTEINS; RNA;

BIOLOGY;

DNA; PROTEIN; RNA POLYMERASE;

AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; ENZYME ACTIVITY; EVOLUTION; GENE MUTATION; GENOTYPE; PHAGE ASSISTED CONTINUOUS EVOLUTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS;

BACTERIOPHAGE T7; BASE SEQUENCE; DNA, VIRAL; DNA-DIRECTED RNA POLYMERASES; EVOLUTION, MOLECULAR; MODELS, BIOLOGICAL; MODELS, GENETIC; MODELS, MOLECULAR; MUTATION RATE; PROMOTER REGIONS, GENETIC; SELECTION, GENETIC; VIRAL PROTEINS;

EID: 84874410798     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3016185     Document Type: Article

References (58)

1. Vasserot, A. P., Dickinson, C. D., Tang, Y., Huse, W. D., Manchester, K. S., and Watkins, J. D. (2003) Optimization of protein therapeutics by directed evolution Drug Discovery Today 8, 118-126
2. Turner, N. J. (2009) Directed evolution drives the next generation of biocatalysts Nat. Chem. Biol. 5, 567-573
3. Hancock, S. M., Rich, J. R., Caines, M. E., Strynadka, N. C., and Withers, S. G. (2009) Designer enzymes for glycosphingolipid synthesis by directed evolution Nat. Chem. Biol. 5, 508-514
4. Gupta, R. D., Goldsmith, M., Ashani, Y., Simo, Y., Mullokandov, G., Bar, H., Ben-David, M., Leader, H., Margalit, R., Silman, I., Sussman, J. L., and Tawfik, D. S. (2011) Directed evolution of hydrolases for prevention of G-type nerve agent intoxication Nat. Chem. Biol. 7, 120-125
5. Bornscheuer, U. T., Huisman, G. W., Kazlauskas, R. J., Lutz, S., Moore, J. C., and Robins, K. (2012) Engineering the third wave of biocatalysis Nature 485, 185-194
6. Bawazer, L. A., Izumi, M., Kolodin, D., Neilson, J. R., Schwenzer, B., and Morse, D. E. (2012) Evolutionary selection of enzymatically synthesized semiconductors from biomimetic mineralization vesicles Proc. Natl. Acad. Sci. U.S.A. 109, E1705-E1714
7. Lunzer, M., Miller, S. P., Felsheim, R., and Dean, A. M. (2005) The biochemical architecture of an ancient adaptive landscape Science 310, 499-501
8. Weinreich, D. M., Delaney, N. F., Depristo, M. A., and Hartl, D. L. (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins Science 312, 111-114
9. Dean, A. M. and Thornton, J. W. (2007) Mechanistic approaches to the study of evolution: The functional synthesis Nat. Rev. Genet. 8, 675-688
10. O'Maille, P. E., Malone, A., Dellas, N., Andes Hess, B., Jr., Smentek, L., Sheehan, I., Greenhagen, B. T., Chappell, J., Manning, G., and Noel, J. P. (2008) Quantitative exploration of the catalytic landscape separating divergent plant sesquiterpene synthases Nat. Chem. Biol. 4, 617-623
11. Romero, P. A. and Arnold, F. H. (2009) Exploring protein fitness landscapes by directed evolution Nat. Rev. Mol. Cell Biol. 10, 866-876
12. Salverda, M. L., Dellus, E., Gorter, F. A., Debets, A. J., van der Oost, J., Hoekstra, R. F., Tawfik, D. S., and de Visser, J. A. (2011) Initial mutations direct alternative pathways of protein evolution PLoS Genet. 7, e1001321
13. Gumulya, Y., Sanchis, J., and Reetz, M. T. (2012) Many pathways in laboratory evolution can lead to improved enzymes: How to escape from local minima ChemBioChem 13, 1060-1066
14. Ghadessy, F. J., Ong, J. L., and Holliger, P. (2001) Directed evolution of polymerase function by compartmentalized self-replication Proc. Natl. Acad. Sci. U.S.A. 98, 4552-4557
15. Barlow, M. and Hall, B. G. (2003) Experimental prediction of the evolution of cefepime resistance from the CMY-2 AmpC β-lactamase Genetics 164, 23-29
16. Cooper, T. F., Rozen, D. E., and Lenski, R. E. (2003) Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 100, 1072-1077
17. Meyer, J. R., Dobias, D. T., Weitz, J. S., Barrick, J. E., Quick, R. T., and Lenski, R. E. (2012) Repeatability and contingency in the evolution of a key innovation in phage lambda Science 335, 428-432
18. Elena, S. F. and Lenski, R. E. (2003) Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation Nat. Rev. Genet. 4, 457-469
19. Elena, S. F., Agudelo-Romero, P., Carrasco, P., Codoner, F. M., Martin, S., Torres-Barcelo, C., and Sanjuan, R. (2008) Experimental evolution of plant RNA viruses Heredity 100, 478-483
20. Tenaillon, O., Rodriguez-Verdugo, A., Gaut, R. L., McDonald, P., Bennett, A. F., Long, A. D., and Gaut, B. S. (2012) The molecular diversity of adaptive convergence Science 335, 457-461
21. Elena, S. F., Wilke, C. O., Ofria, C., and Lenski, R. E. (2007) Effects of population size and mutation rate on the evolution of mutational robustness Evolution 61, 666-674
22. Zwart, M. P., Daros, J. A., and Elena, S. F. (2011) One is enough: In vivo effective population size is dose-dependent for a plant RNA virus PLoS Pathog. 7, e1002122
23. Vignuzzi, M. and Andino, R. (2012) Closing the gap: The challenges in converging theoretical, computational, experimental and real-life studies in virus evolution Curr. Opin. Virol. 2, 515-518
24. Woods, R. J., Barrick, J. E., Cooper, T. F., Shrestha, U., Kauth, M. R., and Lenski, R. E. (2011) Second-order selection for evolvability in a large Escherichia coli population Science 331, 1433-1436
25. Husimi, Y. (1989) Selection and evolution of bacteriophages in cellstat Adv. Biophys. 25, 1-43
26. Bull, J. J. and Molineux, I. J. (2008) Predicting evolution from genomics: Experimental evolution of bacteriophage T7 Heredity 100, 453-463
27. Barrick, J. E., Yu, D. S., Yoon, S. H., Jeong, H., Oh, T. K., Schneider, D., Lenski, R. E., and Kim, J. F. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli Nature 461, 1243-1247
28. Pande, J., Szewczyk, M. M., and Grover, A. K. (2010) Phage display: Concept, innovations, applications and future Biotechnol. Adv. 28, 849-858
29. Breaker, R. R. and Joyce, G. F. (1994) Emergence of a replicating species from an in vitro RNA evolution reaction Proc. Natl. Acad. Sci. U.S.A. 91, 6093-6097
30. Wright, M. C. and Joyce, G. F. (1997) Continuous in vitro evolution of catalytic function Science 276, 614-617
31. Lincoln, T. A. and Joyce, G. F. (2009) Self-sustained replication of an RNA enzyme Science 323, 1229-1232
32. Sczepanski, J. T. and Joyce, G. F. (2012) Synthetic evolving systems that implement a user-specified genetic code of arbitrary design Chem. Biol. 19, 1324-1332
33. Esvelt, K. M., Carlson, J. C., and Liu, D. R. (2011) A system for the continuous directed evolution of biomolecules Nature 472, 499-503
34. Bornscheuer, U. T., Altenbuchner, J., and Meyer, H. H. (1998) Directed evolution of an esterase for the stereoselective resolution of a key intermediate in the synthesis of epothilones Biotechnol. Bioeng. 58, 554-559
35. Carr, R., Alexeeva, M., Dawson, M. J., Gotor-Fernandez, V., Humphrey, C. E., and Turner, N. J. (2005) Directed evolution of an amine oxidase for the preparative deracemisation of cyclic secondary amines ChemBioChem 6, 637-639
36. Gibson, D. G., Young, L., Chuang, R. Y., Venter, J. C., Hutchison, C. A., III, and Smith, H. O. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases Nat. Methods 6, 343-345
37. Summers, W. C. and Siegel, R. B. (1970) Transcription of late phage RNA by T7 RNA polymerase Nature 228, 1160-1162
38. Ikeda, R. A., Chang, L. L., and Warshamana, G. S. (1993) Selection and characterization of a mutant T7 RNA polymerase that recognizes an expanded range of T7 promoter-like sequences Biochemistry 32, 9115-9124
39. Raskin, C. A., Diaz, G. A., and McAllister, W. T. (1993) T7 RNA polymerase mutants with altered promoter specificities Proc. Natl. Acad. Sci. U.S.A. 90, 3147-3151
40. Twigg, A. J. and Sherratt, D. (1980) Trans-complementable copy-number mutants of plasmid ColE1 Nature 283, 216-218
41. Stoker, N. G., Fairweather, N. F., and Spratt, B. G. (1982) Versatile low-copy-number plasmid vectors for cloning in Escherichia coli Gene 18, 335-341
42. Drake, J. W. (1991) A constant rate of spontaneous mutation in DNA-based microbes Proc. Natl. Acad. Sci. U.S.A. 88, 7160-7164
43. Chelliserrykattil, J. and Ellington, A. D. (2004) Evolution of a T7 RNA polymerase variant that transcribes 2′-O-methyl RNA Nat. Biotechnol. 22, 1155-1160
44. Nei, M. and Chesser, R. K. (1983) Estimation of fixation indices and gene diversities Ann. Hum. Genet. 47, 253-259
45. Holsinger, K. E. and Weir, B. S. (2009) Genetics in geographically structured populations: Defining, estimating and interpreting F(ST) Nat. Rev. Genet. 10, 639-650
46. Cheetham, G. M. and Steitz, T. A. (1999) Structure of a transcribing T7 RNA polymerase initiation complex Science 286, 2305-2309
47. Steitz, T. A. (2009) The structural changes of T7 RNA polymerase from transcription initiation to elongation Curr. Opin. Struct. Biol. 19, 683-690
48. Yin, Y. W. and Steitz, T. A. (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase Science 298, 1387-1395
49. Poelwijk, F. J., Kiviet, D. J., Weinreich, D. M., and Tans, S. J. (2007) Empirical fitness landscapes reveal accessible evolutionary paths Nature 445, 383-386
50. Tahirov, T. H., Temiakov, D., Anikin, M., Patlan, V., McAllister, W. T., Vassylyev, D. G., and Yokoyama, S. (2002) Structure of a T7 RNA polymerase elongation complex at 2.9 Å resolution Nature 420, 43-50
51. Tokuriki, N. and Tawfik, D. S. (2009) Stability effects of mutations and protein evolvability Curr. Opin. Struct. Biol. 19, 596-604
52. Bloom, J. D., Labthavikul, S. T., Otey, C. R., and Arnold, F. H. (2006) Protein stability promotes evolvability Proc. Natl. Acad. Sci. U.S.A. 103, 5869-5874
53. Drummond, D. A., Iverson, B. L., Georgiou, G., and Arnold, F. H. (2005) Why high-error-rate random mutagenesis libraries are enriched in functional and improved proteins J. Mol. Biol. 350, 806-816
54. Bershtein, S. and Tawfik, D. S. (2008) Ohno's model revisited: Measuring the frequency of potentially adaptive mutations under various mutational drifts Mol. Biol. Evol. 25, 2311-2318
55. Pollock, D. D., Thiltgen, G., and Goldstein, R. A. (2012) Amino acid coevolution induces an evolutionary Stokes shift Proc. Natl. Acad. Sci. U.S.A. 109, E1352-E1359
56. Bershtein, S., Goldin, K., and Tawfik, D. S. (2008) Intense neutral drifts yield robust and evolvable consensus proteins J. Mol. Biol. 379, 1029-1044
57. Wang, X., Minasov, G., and Shoichet, B. K. (2002) Evolution of an antibiotic resistance enzyme constrained by stability and activity trade-offs J. Mol. Biol. 320, 85-95
58. Jackel, C., Kast, P., and Hilvert, D. (2008) Protein design by directed evolution Annu. Rev. Biophys. 37, 153-173