Directed evolution of Escherichia coli with lower-than-natural plasmid mutation rates

Nucleic Acids Research

Volumn 46, Issue 17, 2018, Pages 9236-9250

  Deatherage, Daniel E ^a   Leon, Dacia ^a   Rodriguez, Álvaro E ^a   Omar, Salma K ^a   Barrick, Jeffrey E ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; RIBONUCLEASE E; BACTERIAL DNA; ESCHERICHIA COLI PROTEIN; RIBONUCLEASE;

ARTICLE; BACTERIAL CHROMOSOME; CONTROLLED STUDY; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; GENE DOSAGE; GENE EXPRESSION; GENETIC STABILITY; GROWTH RATE; MUTATION RATE; NONHUMAN; PLASMID; POLA GENE; POLB GENE; PRIORITY JOURNAL; RNE GENE; CHEMISTRY; COPY NUMBER VARIATION; DNA REPLICATION; DNA SEQUENCE; GENETIC ENGINEERING; GENETIC SELECTION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROCEDURES; RADIATION RESPONSE; SYNTHETIC BIOLOGY; ULTRAVIOLET RADIATION;

BASE SEQUENCE; DIRECTED MOLECULAR EVOLUTION; DNA COPY NUMBER VARIATIONS; DNA POLYMERASE I; DNA REPLICATION; DNA, BACTERIAL; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC ENGINEERING; MUTATION RATE; PLASMIDS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SYNTHETIC BIOLOGY; ULTRAVIOLET RAYS;

EID: 85054421094     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gky751     Document Type: Article

References (88)

1. Teng,X., Dayhoff-Brannigan,M., Cheng,W.-C., Gilbert,C.E., Sing,C.N., Diny,N.L., Wheelan,S.J., Dunham,M.J., Boeke,J.D., Pineda,F.J. et al. (2013) Genome-wide consequences of deleting any single gene. Mol. Cell, 52, 485–494.
2. Sandoval,C.M., Ayson,M., Moss,N., Lieu,B., Jackson,P., Gaucher,S.P., Horning,T., Dahl,R.H., Denery,J.R., Abbott,D.A. et al. (2014) Use of pantothenate as a metabolic switch increases the genetic stability of farnesene producing Saccharomyces cerevisiae. Metab. Eng., 25, 1–12.
3. Gibson,D.G., Glass,J.I., Lartigue,C., Noskov,V.N., Chuang,R.-Y., Algire,M.A., Benders,G.A., Montague,M.G., Ma,L., Moodie,M.M. et al. (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science, 329, 52–56.
4. Wannier,T.M., Kunjapur,A.M., Rice,D.P., McDonald,M.J., Desai,M.M. and Church,G.M. (2018) Adaptive evolution of genomically recoded Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 115, 3090–3095.
5. Bull,J.J. and Barrick,J.E. (2017) Arresting evolution. Trends Genet., 33, 910–920.
6. Scott,M., Gunderson,C.W, Mateescu,E.M., Zhang,Z. and Hwa,T. (2010) Interdependence of cell growth and gene expression: origins and consequences. Science, 330, 1099–1102.
7. Borkowski,O., Ceroni,F., Stan,G.-B. and Ellis,T. (2016) Overloaded and stressed: whole-cell considerations for bacterial synthetic biology. Curr. Opin. Microbiol., 33, 123–130.
8. Canton,B., Labno,A. and Endy,D. (2008) Refinement and standardization of synthetic biological parts and devices. Nat. Biotechnol., 26, 787–793.
9. Renda,B.A., Hammerling,M.J. and Barrick,J.E. (2014) Engineering reduced evolutionary potential for synthetic biology. Mol. Biosyst., 10, 1668–1678.
10. Arkin,A.P. and Fletcher,D.A. (2006) Fast, cheap and somewhat in control. Genome Biol., 7, 114.
11. Pósfai,G., Plunkett,G., Fehér,T., Frisch,D., Keil,G.M., Umenhoffer,K., Kolisnychenko,V., Stahl,B., Sharma,S.S., de Arruda,M. et al. (2006) Emergent properties of reduced-genome Escherichia coli. Science, 312, 1044–1046.
12. Csörgo,B., Fehér,T., Tímár,E., Blattner,F.R. and Pósfai,G. (2012) Low-mutation-rate, reduced-genome Escherichia coli: an improved host for faithful maintenance of engineered genetic constructs. Microb. Cell Fact., 11, 11.
13. Jack,B.R., Leonard,S.P., Mishler,D.M., Renda,B.A., Leon,D., Suárez,G.A. and Barrick,J.E. (2014) Predicting the genetic stability of engineered DNA sequences with the EFM calculator. ACS Synth. Biol., 4, 939–943.
14. Suárez,G.A., Renda,B.A., Dasgupta,A. and Barrick,J.E. (2017) Reduced mutation rate and increased transformability of transposon-free Acinetobacter baylyi ADP1-ISx. Appl. Environ. Microbiol., 83, e01025-17.
15. Choi,J.W., Yim,S.S., Kim,M.J. and Jeong,K.J. (2015) Enhanced production of recombinant proteins with Corynebacterium glutamicum by deletion of insertion sequences (IS elements). Microb. Cell Fact., 14, 207.
16. Rugbjerg,P., Myling-Petersen,N., Porse,A., Sarup-Lytzen,K. and Sommer,M.O.A. (2018) Diverse genetic error modes constrain large-scale bio-based production. Nat. Commun., 9, 787.
17. Ceroni,F., Algar,R., Stan,G.-B. and Ellis,T. (2015) Quantifying cellular capacity identifies gene expression designs with reduced burden. Nat. Methods, 12, 415–418.
18. Romero,P.A. and Arnold,F.H. (2009) Exploring protein fitness landscapes by directed evolution. Nat. Rev. Mol. Cell Biol., 10, 866–876.
19. Haseltine,E.L. and Arnold,F.H. (2007) Synthetic gene circuits: design with directed evolution. Annu. Rev. Biophys. Biomol. Struct., 36, 1–19.
20. Baba,T., Ara,T., Hasegawa,M., Takai,Y., Okumura,Y., Baba,M., Datsenko,K.A., Tomita,M., Wanner,B.L. and Mori,H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol., 2, 2006.0008.
21. Sleight,S.C., Bartley,B.A., Lieviant,J.A. and Sauro,H.M. (2010) Designing and engineering evolutionary robust genetic circuits. J. Biol. Eng., 4, 12.
22. Tack,D.S., Ellefson,J.W., Thyer,R., Wang,B., Gollihar,J., Forster,M.T. and Ellington,A.D. (2016) Addicting diverse bacteria to a noncanonical amino acid. Nat. Chem. Biol., 12, 138–140.
23. Ellis,B., Haaland,P., Hahne,F., Le Meur,N., Gopalakrishnan,N., Spidlen,J. and Jiang,M. (2018) flowCore: Basic structures for flow cytometry data. R package version 1.42.3.
24. Deatherage,D.E. and Barrick,J.E. (2014) Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol. Biol., 1151, 165–188.
25. Nehring,R.B., Gu,F., Lin,H.Y., Gibson,J.L., Blythe,M.J., Wilson,R., Bravo Núñez,M.A., Hastings,P.J., Louis,E.J., Frisch,R.L. et al. (2015) An ultra-dense library resource for rapid deconvolution of mutations that cause phenotypes in Escherichia coli. Nucleic Acids Res., 44, 1–11.
26. Thomason,L.C., Costantino,N. and Court,D.L. (2007) E. coli genome manipulation by P1 transduction. Curr. Protoc. Mol. Biol., doi:10.1002/0471142727.mb0117s79.
27. Datsenko,K.A. and Wanner,B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A., 97, 6640–6645.
28. Rosche,W.A. and Foster,P.L. (2000) Determining mutation rates in bacterial populations. Methods, 20, 4–17.
29. Jin,D.J. and Zhou,Y.N. (1996) Mutational analysis of structure-function relationship of RNA polymerase in Escherichia coli. Methods Enzymol., 273, 300–319.
30. Fehér,T., Cseh,B., Umenhoffer,K., Karcagi,I. and Pósfai,G. (2006) Characterization of cycA mutants of Escherichia coli. An assay for measuring in vivo mutation rates. Mutat. Res., 595, 184–190.
31. Zheng,Q. (2017) rSalvador: An R package for the fluctuation experiment. G3 (Bethesda), 7, 3849–3856.
32. Lee,C., Kim,J., Shin,S.G. and Hwang,S. (2006) Absolute and relative QPCR quantification of plasmid copy number in Escherichia coli. J. Biotechnol., 123, 273–280.
33. Wang,F. and Yang,W. (2009) Structural insight into translesion synthesis by DNA Pol II. Cell, 139, 1279–1289.
34. Lin-Chao,S. and Cohen,S.N. (1991) The rate of processing and degradation of antisense RNAI regulates the replication of ColE1-type plasmids in vivo. Cell, 65, 1233–1242.
35. Kües,U. and Stahl,U. (1989) Replication of plasmids in gram-negative bacteria. Microbiol. Rev., 53, 491–516.
36. Tomcsányi,T. and Apirion,D. (1985) Processing enzyme ribonuclease E specifically cleaves RNA I. An inhibitor of primer formation in plasmid DNA synthesis. J. Mol. Biol., 185, 713–720.
37. Callaghan,A.J., Marcaida,M.J., Stead,J.A., McDowall,K.J., Scott,W.G. and Luisi,B.F. (2005) Structure of Escherichia coli RNase E catalytic domain and implications for RNA turnover. Nature, 437, 1187–1191.
38. Loh,E., Choe,J. and Loeb,L.A. (2007) Highly tolerated amino acid substitutions increase the fidelity of Escherichia coli DNA polymerase I. J. Biol. Chem., 282, 12201–12209.
39. Beese,L.S., Friedman,J.M. and Steitz,T.A. (1993) Crystal structures of the Klenow fragment of DNA polymerase I complexed with deoxynucleoside triphosphate and pyrophosphate. Biochemistry, 32, 14095–14101.
40. Eyre-Walker,A. and Keightley,P.D. (2007) The distribution of fitness effects of new mutations. Nat. Rev. Genet., 8, 610–618.
41. Bataillon,T. and Bailey,S.F. (2014) Effects of new mutations on fitness: Insights from models and data. Ann. N.Y. Acad. Sci., 1320, 76–92.
42. Robert,L., Ollion,J., Robert,J., Song,X., Matic,I. and Elez,M. (2018) Mutation dynamics and fitness effects followed in single cells. Science, 359, 1283–1286.
43. Sniegowski,P.D., Gerrish,P.J., Johnson,T. and Shaver,A. (2000) The evolution of mutation rates: separating causes from consequences. BioEssays, 22, 1057–1066.
44. de Visser,J.A.G.M. (2002) The fate of microbial mutators. Microbiology, 148, 1247–1252.
45. Denamur,E. and Matic,I. (2006) Evolution of mutation rates in bacteria. Mol. Microbiol., 60, 820–827.
46. Voordeckers,K., Kominek,J., Das,A., Espinosa-Cantú,A., De Maeyer,D., Arslan,A., Van Pee,M., van der Zande,E., Meert,W., Yang,Y. et al. (2015) Adaptation to high ethanol reveals complex evolutionary pathways. PLoS Genet., 11, e1005635.
47. Sniegowski,P.D., Gerrish,P.J. and Lenski,R.E. (1997) Evolution of high mutation rates in experimental populations of E. coli. Nature, 387, 703–705.
48. Tenaillon,O., Taddei,F., Radmian,M. and Matic,I. (2001) Second-order selection in bacterial evolution: selection acting on mutation and recombination rates in the course of adaptation. Res. Microbiol., 152, 11–16.
49. Barrick,J.E. and Lenski,R.E. (2013) Genome dynamics during experimental evolution. Nat. Rev. Genet., 14, 827–839.
50. Funchain,P., Yeung,A., Stewart,J.L., Lin,R., Slupska,M.M. and Miller,J.H. (2000) The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics, 154, 959–970.
51. Leiby,N. and Marx,C.J. (2014) Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biol., 12, e1001789.
52. Marvig,R.L., Sommer,L.M., Molin,S. and Johansen,H.K. (2015) Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nat. Genet., 47, 57–64.
53. Oliver,A. and Mena,A. (2010) Bacterial hypermutation in cystic fibrosis, not only for antibiotic resistance. Clin. Microbiol. Infect., 16, 798–808.
54. Oliver,A., Cantón,R., Campo,P., Baquero,F. and Blázquez,J. (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science, 288, 1251–1254.
55. Couce,A., Caudwell,L.V., Feinauer,C., Hindré,T., Feugeas,J.-P., Weigt,M., Lenski,R.E., Schneider,D. and Tenaillon,O. (2017) Mutator genomes decay, despite sustained fitness gains, in a long-term experiment with bacteria. Proc. Natl. Acad. Sci. U.S.A., 114, E9026–E9035.
56. McDonald,M.J., Hsieh,Y.Y., Yu,Y.H., Chang,S.L. and Leu,J.Y. (2012) The evolution of low mutation rates in experimental mutator populations of Saccharomyces cerevisiae. Curr. Biol., 22, 1235–1240.
57. Sprouffske,K., Aguilar-Rodríguez,J., Sniegowski,P. and Wagner,A. (2018) High mutation rates limit evolutionary adaptation in Escherichia coli. PLoS Genet., 14, e1007324.
58. Wielgoss,S., Barrick,J.E., Tenaillon,O., Wiser,M.J., Dittmar,W.J., Cruveiller,S., Chane-Woon-Ming,B., Médigue,C., Lenski,R.E. and Schneider,D. (2013) Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proc. Natl. Acad. Sci. U.S.A., 110, 222–227.
59. Tenaillon,O., Barrick,J.E., Ribeck,N., Deatherage,D.E., Blanchard,J.L., Dasgupta,A., Wu,G.C., Wielgoss,S., Cruveiller,S., Médigue,C. et al. (2016) Tempo and mode of genome evolution in a 50,000-generation experiment. Nature, 536, 165–170.
60. Drake,J.W. (1991) A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. U.S.A., 88, 7160–7164.
61. Lynch,M. (2010) Evolution of the mutation rate. Trends Genet., 26, 345–352.
62. Lynch,M., Ackerman,M.S., Gout,J.-F., Long,H., Sung,W., Thomas,W.K. and Foster,P.L. (2016) Genetic drift, selection and the evolution of the mutation rate. Nat. Rev. Genet., 17, 704–714.
63. Friedberg,E.C., Walker,G.C., Siede,W., Wood,R.D., Schultz,R.A. and Ellenberger,T. (2006) DNA Repair and Mutagenesis. 2nd edn. ASM Press, Washington, DC.
64. Galperin,M.Y., Moroz,O.V., Wilson,K.S. and Murzin,A.G. (2006) House cleaning, a part of good housekeeping. Mol. Microbiol., 59, 5–19.
65. Quiñones,A. and Piechocki,R. (1985) Isolation and characterization of Escherichia coli antimutators. A new strategy to study the nature and origin of spontaneous mutations. Mol. Gen. Genet., 201, 315–322.
66. Fijalkowska,I.J., Dunn,R.L. and Schaaper,R.M. (1993) Mutants of Escherichia coli with increased fidelity of DNA replication. Genetics, 134, 1023–1030.
67. Oller,A.R. and Schaaper,R.M. (1994) Spontaneous mutation in Escherichia coli containing the dnaE911 DNA polymerase antimutator allele. Genetics, 138, 263–270.
68. Kamiya,H., Iida,E., Murata-Kamiya,N., Yamamoto,Y., Miki,T. and Harashima,H. (2003) Suppression of spontaneous and hydrogen peroxide-induced mutations by a MutT-type nucleotide pool sanitization enzyme, the Escherichia coli Orf135 protein. Genes Cells, 8, 941–950.
69. Fujikawa,K. and Kasai,H. (2002) The oxidized pyrimidine ribonucleotide, 5-hydroxy-CTP, is hydrolyzed efficiently by the Escherichia coli recombinant Orf135 protein. DNA Repair (Amst.), 1, 571–576.
70. Camps,M., Naukkarinen,J., Johnson,B.P. and Loeb,L.A. (2003) Targeted gene evolution in Escherichia coli using a highly error-prone DNA polymerase I. Proc. Natl. Acad. Sci. U.S.A., 100, 9727–9732.
71. Loh,E., Salk,J.J. and Loeb,L.A. (2010) Optimization of DNA polymerase mutation rates during bacterial evolution. Proc. Natl. Acad. Sci. U.S.A., 107, 1154–1159.
72. Yang,Y.L. and Polisky,B. (1993) Suppression of ColE1 high-copy-number mutants by mutations in the polA gene of Escherichia coli. J. Bacteriol., 175, 428–437.
73. Frisch,R.L., Su,Y., Thornton,P.C., Gibson,J.L., Rosenberg,S.M. and Hastings,P.J. (2010) Separate DNA Pol II- and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. J. Bacteriol., 192, 4694–4700.
74. Dapa,T., Fleurier,S., Bredeche,M.-F. and Matic,I. (2017) The SOS and RpoS regulons contribute to bacterial cell robustness to genotoxic stress by synergistically regulating DNA polymerase Pol II. Genetics, 206, 1349–1360.
75. Witkin,E.M. (1976) Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol. Rev., 40, 869–907.
76. Janel-Bintz,R., Napolitano,R.L., Isogawa,A., Fujii,S. and Fuchs,R.P. (2017) Processing closely spaced lesions during Nucleotide Excision Repair triggers mutagenesis in E. coli. PLoS Genet., 13, e1006881.
77. Escarceller,M., Hicks,J., Gudmundsson,G., Trump,G., Touati,D., Lovett,S., Foster,P.L., McEntee,K. and Goodman,M.F. (1994) Involvement of Escherichia coli DNA polymerase II in response to oxidative damage and adaptive mutation. J. Bacteriol., 176, 6221–6228.
78. Hastings,P.J., Hersh,M.N., Thornton,P.C., Fonville,N.C., Slack,A., Frisch,R.L., Ray,M.P., Harris,R.S., Leal,S.M. and Rosenberg,S.M. (2010) Competition of Escherichia coli DNA polymerases I, II and III with DNA Pol IV in stressed cells. PLoS One, 5, e10862.
79. Napolitano,R., Janel-Bintz,R., Wagner,J. and Fuchs,R.P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis. EMBO J., 19, 6259–6265.
80. Wagner,J., Etienne,H., Janel-Bintz,R. and Fuchs,R.P.P. (2002) Genetics of mutagenesis in E. coli: Various combinations of translesion polymerases (Pol II, IV and V) deal with lesion/sequence context diversity. DNA Repair (Amst)., 1, 159–167.
81. Cirz,R.T., Chin,J.K., Andes,D.R., De Crécy-Lagard,V., Craig,W.A. and Romesberg,F.E. (2005) Inhibition of mutation and combating the evolution of antibiotic resistance. PLoS Biol., 3, 1024–1033.
82. Mohanty,B.K. and Kushner,S.R. (2016) Regulation of mRNA decay in bacteria. Annu. Rev. Microbiol., 70, 25–44.
83. Stead,M.B., Marshburn,S., Mohanty,B.K., Mitra,J., Pena Castillo,L., Ray,D., van Bakel,H., Hughes,T.R. and Kushner,S.R. (2011) Analysis of Escherichia coli RNase E and RNase III activity in vivo using tiling microarrays. Nucleic Acids Res., 39, 3188–3203.
84. ´ Papenfort,K., Reinhardt,R., Wieden,H.-J. et al. (2017) In vivo cleavage map illuminates the central role of RNase E in coding and non-coding RNA pathways. Mol. Cell, 65, 39–51.
85. Gottesman,S., McCullen,C.A., Guillier,M., Vanderpool,C.K., Majdalani,N., Benhammou,J., Thompson,K.M., FitzGerald,P.C., Sowa,N.A. and FitzGerald,D.J. (2006) Small RNA regulators and the bacterial response to stress. Cold Spring Harb. Symp. Quant. Biol., 71, 1–11.
86. Wang,H.H., Isaacs,F.J., Carr,P.A., Sun,Z.Z., Xu,G., Forest,C.R. and Church,G.M. (2009) Programming cells by multiplex genome engineering and accelerated evolution. Nature, 460, 894–898.
87. Garst,A.D., Bassalo,M.C., Pines,G., Lynch,S.A., Halweg-Edwards,A.L., Liu,R., Liang,L., Wang,Z., Zeitoun,R., Alexander,W.G. et al. (2017) Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering. Nat. Biotechnol., 35, 48–55.
88. Umenhoffer,K., Fehér,T., Balikó,G., Ayaydin,F., Pósfai,J., Blattner,F.R. and Pósfai,G. (2010) Reduced evolvability of Escherichia coli MDS42, an IS-less cellular chassis for molecular and synthetic biology applications. Microb. Cell Fact., 9, 38.