Memory and Combinatorial Logic Based on DNA Inversions: Dynamics and Evolutionary Stability

ACS Synthetic Biology

Volumn 4, Issue 12, 2015, Pages 1361-1372

  Fernandez Rodriguez, Jesus ^a   Yang, Lei ^a   Gorochowski, Thomas E ^a   Gordon, D Benjamin ^a,b   Voigt, Christopher A ^a,b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

design automation; genetic circuit; genetic compiler; synthetic biology; systems biology

Indexed keywords

ARABINOSE; BETA FRUCTOFURANOSIDASE; DNA; GENOMIC DNA; PLASMID DNA; RECOMBINASE; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; FIME PROTEIN, E COLI; HBIF PROTEIN, E COLI;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA PURIFICATION; DNA REPLICATION ORIGIN; DNA SEQUENCE; FLOW CYTOMETRY; GENE EXPRESSION; GENE SEQUENCE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; CHEMISTRY; CHROMOSOME INVERSION; LOGIC; MOLECULAR COMPUTER;

COMPUTERS, MOLECULAR; DNA; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; LOGIC; RECOMBINASES; SEQUENCE INVERSION;

EID: 84952684288     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.5b00170     Document Type: Article

References (111)

1. Sternberg, N. and Hamilton, D. (1981) Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites J. Mol. Biol. 150, 467-486 10.1016/0022-2836(81)90375-2
2. Kunkel, B., Losick, R., and Stragier, P. (1990) The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene Genes Dev. 4, 525-535 10.1101/gad.4.4.525
3. Carrasco, C. D. and Golden, J. W. (1995) Two heterocyst-specific DNA rearrangements of nif operons in Anabaena cylindrica and Nostoc sp. strain Mac Microbiology 141, 2479-2487 10.1099/13500872-141-10-2479
4. Klemm, P., Jørgensen, B. J., Die, I., van Ree, H., and de Bergmans, H. (1985) The fim genes responsible for synthesis of type 1 fimbriae in Escherichia coli, cloning and genetic organization Mol. Gen. Genet. 199, 410-414 10.1007/BF00330751
5. Abraham, J. M., Freitag, C. S., Clements, J. R., and Eisenstein, B. I. (1985) An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 82, 5724-5727 10.1073/pnas.82.17.5724
6. Grindley, N. D. F., Whiteson, K. L., and Rice, P. A. (2006) Mechanisms of Site-Specific Recombination∗ Annu. Rev. Biochem. 75, 567-605 10.1146/annurev.biochem.73.011303.073908
7. Johnson, R. C. and Simon, M. I. (1985) Hin-mediated site-specific recombination requires two 26 bp recombination sites and a 60 bp recombinational enhancer Cell 41, 781-791 10.1016/S0092-8674(85)80059-3
8. Dybvig, K. and Yu, H. (1994) Regulation of a restriction and modification system via DNA inversion in Mycoplasma pulmonis Mol. Microbiol. 12, 547-560 10.1111/j.1365-2958.1994.tb01041.x
9. Lenich, A. G. and Glasgow, A. C. (1994) Amino acid sequence homology between Piv, an essential protein in site-specific DNA inversion in Moraxella lacunata, and transposases of an unusual family of insertion elements J. Bacteriol. 176, 4160-4164
10. Dworkin, J. and Blaser, M. J. (1996) Generation of Campylobacter fetus S-layer protein diversity utilizes a single promoter on an invertible DNA segment Mol. Microbiol. 19, 1241-1253 10.1111/j.1365-2958.1996.tb02469.x
11. Zhao, H., Li, X., Johnson, D. E., Blomfield, I., and Mobley, H. L. (1997) In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract Mol. Microbiol. 23, 1009-1019 10.1046/j.1365-2958.1997.2791645.x
12. Weinacht, K. G., Roche, H., Krinos, C. M., Coyne, M. J., Parkhill, J., and Comstock, L. E. (2004) Tyrosine site-specific recombinases mediate DNA inversions affecting the expression of outer surface proteins of Bacteroides fragilis Mol. Microbiol. 53, 1319-1330 10.1111/j.1365-2958.2004.04219.x
13. Ham, T. S., Lee, S. K., Keasling, J. D., and Arkin, A. P. (2006) A tightly regulated inducible expression system utilizing the fim inversion recombination switch Biotechnol. Bioeng. 94, 1-4 10.1002/bit.20916
14. Moon, T. S., Clarke, E. J., Groban, E. S., Tamsir, A., Clark, R. M., Eames, M., Kortemme, T., and Voigt, C. A. (2011) Construction of a genetic multiplexer to toggle between chemosensory pathways in Escherichia coli J. Mol. Biol. 406, 215-227 10.1016/j.jmb.2010.12.019
15. Friedland, A. E., Lu, T. K., Wang, X., Shi, D., Church, G., and Collins, J. J. (2009) Synthetic Gene Networks That Count Science 324, 1199-1202 10.1126/science.1172005
16. Baumgardner, J., Acker, K., Adefuye, O., Crowley, S. T., DeLoache, W., Dickson, J. O., Heard, L., Martens, A. T., Morton, N., Ritter, M., Shoecraft, A., Treece, J., Unzicker, M., Valencia, A., Waters, M., Campbell, A. M., Heyer, L. J., Poet, J. L., and Eckdahl, T. T. (2009) Solving a Hamiltonian Path Problem with a bacterial computer J. Biol. Eng. 3, 11 10.1186/1754-1611-3-11
17. Haynes, K. A., Broderick, M. L., Brown, A. D., Butner, T. L., Dickson, J. O., Harden, W. L., Heard, L. H., Jessen, E. L., Malloy, K. J., Ogden, B. J., Rosemond, S., Simpson, S., Zwack, E., Campbell, A. M., Eckdahl, T. T., Heyer, L. J., and Poet, J. L. (2008) Engineering bacteria to solve the Burnt Pancake Problem J. Biol. Eng. 2, 8 10.1186/1754-1611-2-8
18. Bonnet, J., Yin, P., Ortiz, M. E., Subsoontorn, P., and Endy, D. (2013) Amplifying Genetic Logic Gates Science 340, 599-603 10.1126/science.1232758
19. Archer, E. J., Robinson, A. B., and Süel, G. M. (2012) Engineered E. coli That Detect and Respond to Gut Inflammation through Nitric Oxide Sensing ACS Synth. Biol. 1, 451-457 10.1021/sb3000595
20. Mimee, M., Tucker, A. C., Voigt, C. A., and Lu, T. K. (2015) Programming a Human Commensal Bacterium, Bacteroides thetaiotaomicron, to Sense and Respond to Stimuli in the Murine Gut Microbiota Cell Syst. 1, 62-71 10.1016/j.cels.2015.06.001
21. Piepenburg, O., Williams, C. H., Stemple, D. L., and Armes, N. A. (2006) DNA Detection Using Recombination Proteins PLoS Biol. 4, e204 10.1371/journal.pbio.0040204
22. Krõlov, K., Frolova, J., Tudoran, O., Suhorutsenko, J., Lehto, T., Sibul, H., Mäger, I., Laanpere, M., Tulp, I., and Langel, Ü. (2014) Sensitive and Rapid Detection of Chlamydia trachomatis by Recombinase Polymerase Amplification Directly from Urine Samples J. Mol. Diagn. 16, 127-135 10.1016/j.jmoldx.2013.08.003
23. Yamanishi, M. and Matsuyama, T. (2012) A Modified Cre-lox Genetic Switch To Dynamically Control Metabolic Flow in Saccharomyces cerevisiae ACS Synth. Biol. 1, 172-180 10.1021/sb200017p
24. Araki, H., Jearnpipatkul, A., Tatsumi, H., Sakurai, T., Ushio, K., Muta, T., and Oshima, Y. (1985) Molecular and functional organization of yeast plasmid pSR1 J. Mol. Biol. 182, 191-203 10.1016/0022-2836(85)90338-9
25. McLeod, M., Craft, S., and Broach, J. R. (1986) Identification of the crossover site during FLP-mediated recombination in the Saccharomyces cerevisiae plasmid 2 microns circle Mol. Cell. Biol. 6, 3357-3367 10.1128/MCB.6.10.3357
26. Thorpe, H. M., Wilson, S. E., and Smith, M. C. (2000) Control of directionality in the site-specific recombination system of the Streptomyces phage phiC31 Mol. Microbiol. 38, 232-241 10.1046/j.1365-2958.2000.02142.x
27. Ghosh, P., Wasil, L. R., and Hatfull, G. F. (2006) Control of phage Bxb1 excision by a novel recombination directionality factor PLoS Biol. 4, e186 10.1371/journal.pbio.0040186
28. Brown, W. R. A., Lee, N. C. O., Xu, Z., and Smith, M. C. M. (2011) Serine recombinases as tools for genome engineering Methods 53, 372-379 10.1016/j.ymeth.2010.12.031
29. Yang, L., Nielsen, A. A. K., Fernandez-Rodriguez, J., McClune, C. J., Laub, M. T., Lu, T. K., and Voigt, C. A. (2014) Permanent genetic memory with > 1-byte capacity Nat. Methods 11, 1261-1266 10.1038/nmeth.3147
30. Bonnet, J., Subsoontorn, P., and Endy, D. (2012) Rewritable digital data storage in live cells via engineered control of recombination directionality Proc. Natl. Acad. Sci. U. S. A. 109, 8884-8889 10.1073/pnas.1202344109
31. Siuti, P., Yazbek, J., and Lu, T. K. (2013) Synthetic circuits integrating logic and memory in living cells Nat. Biotechnol. 31, 448-452 10.1038/nbt.2510
32. Brophy, J. A. N. and Voigt, C. A. (2014) Principles of genetic circuit design Nat. Methods 11, 508-520 10.1038/nmeth.2926
33. Yokobayashi, Y., Weiss, R., and Arnold, F. H. (2002) Directed evolution of a genetic circuit Proc. Natl. Acad. Sci. U. S. A. 99, 16587-16591 10.1073/pnas.252535999
34. Lucks, J. B., Qi, L., Mutalik, V. K., Wang, D., and Arkin, A. P. (2011) Versatile RNA-sensing transcriptional regulators for engineering genetic networks Proc. Natl. Acad. Sci. U. S. A. 108, 8617-8622 10.1073/pnas.1015741108
35. Liu, C. C., Qi, L., Lucks, J. B., Segall-Shapiro, T. H., Wang, D., Mutalik, V. K., and Arkin, A. P. (2012) An adaptor from translational to transcriptional control enables predictable assembly of complex regulation Nat. Methods 9, 1088-1094 10.1038/nmeth.2184
36. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., and Lim, W. A. (2013) Repurposing CRISPR as an RNA-Guided Platform for Sequence-Specific Control of Gene Expression Cell 152, 1173-1183 10.1016/j.cell.2013.02.022
37. Nielsen, A. A. and Voigt, C. A. (2014) Multi-input CRISPR/Cas genetic circuits that interface host regulatory networks Mol. Syst. Biol. 10, 763 10.15252/msb.20145735
38. Klemm, P. (1986) Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli EMBO J. 5, 1389-1393
39. Xie, Y., Yao, Y., Kolisnychenko, V., Teng, C.-H., and Kim, K. S. (2006) HbiF Regulates Type 1 Fimbriation Independently of FimB and FimE Infect. Immun. 74, 4039-4047 10.1128/IAI.02058-05
40. iGEM Michigan Synthetic Biology Team. (2012) http://2012.igem.org/Team:Michigan/Project.
41. Gally, D. L., Leathart, J., and Blomfield, I. C. (1996) Interaction of FimB and FimE with the fim switch that controls the phase variation of type 1 fimbriae in Escherichia coli K-12 Mol. Microbiol. 21, 725-738 10.1046/j.1365-2958.1996.311388.x
42. Kulasekara, H. D. and Blomfield, I. C. (1999) The molecular basis for the specificity of fimE in the phase variation of type 1 fimbriae of Escherichia coli K-12 Mol. Microbiol. 31, 1171-1181 10.1046/j.1365-2958.1999.01257.x
43. Holden, N., Blomfield, I. C., Uhlin, B.-E., Totsika, M., Kulasekara, D. H., and Gally, D. L. (2007) Comparative analysis of FimB and FimE recombinase activity Microbiology 153, 4138-4149 10.1099/mic.0.2007/010363-0
44. McClain, M. S., Blomfield, I. C., Eberhardt, K. J., and Eisenstein, B. I. (1993) Inversion-independent phase variation of type 1 fimbriae in Escherichia coli J. Bacteriol. 175, 4335-4344
45. Gally, D. L., Rucker, T. J., and Blomfield, I. C. (1994) The leucine-responsive regulatory protein binds to the fim switch to control phase variation of type 1 fimbrial expression in Escherichia coli K-12 J. Bacteriol. 176, 5665-5672
46. Kuwahara, H., Myers, C. J., and Samoilov, M. S. (2010) Temperature Control of Fimbriation Circuit Switch in Uropathogenic Escherichia coli: Quantitative Analysis via Automated Model Abstraction PLoS Comput. Biol. 6, e1000723 10.1371/journal.pcbi.1000723
47. Bryan, A., Roesch, P., Davis, L., Moritz, R., Pellett, S., and Welch, R. A. (2006) Regulation of Type 1 Fimbriae by Unlinked FimB- and FimE-Like Recombinases in Uropathogenic Escherichia coli Strain CFT073 Infect. Immun. 74, 1072-1083 10.1128/IAI.74.2.1072-1083.2006
48. Blattner, F. R., Plunkett, G., Bloch, C. A., Perna, N. T., Burland, V., Riley, M., Collado-Vides, J., Glasner, J. D., Rode, C. K., Mayhew, G. F., Gregor, J., Davis, N. W., Kirkpatrick, H. A., Goeden, M. A., Rose, D. J., Mau, B., and Shao, Y. (1997) The Complete Genome Sequence of Escherichia coli K-12 Science 277, 1453-1462 10.1126/science.277.5331.1453
49. Endy, D. (2005) Foundations for engineering biology Nature 438, 449-453 10.1038/nature04342
50. Clancy, K. and Voigt, C. A. (2010) Programming cells: towards an automated Genetic Compiler. Curr. Opin. Biotechnol. 21, 572-581 10.1016/j.copbio.2010.07.005
51. Burns, L. S., Smith, S. G. J., and Dorman, C. J. (2000) Interaction of the FimB Integrase with the fimS Invertible DNA Element in Escherichia coli In Vivo and In Vitro J. Bacteriol. 182, 2953-2959 10.1128/JB.182.10.2953-2959.2000
52. Wang, K. H., Sauer, R. T., and Baker, T. A. (2007) ClpS modulates but is not essential for bacterial N-end rule degradation Genes Dev. 21, 403-408 10.1101/gad.1511907
53. Lou, C., Stanton, B., Chen, Y.-J., Munsky, B., and Voigt, C. A. (2012) Ribozyme-based insulator parts buffer synthetic circuits from genetic context Nat. Biotechnol. 30, 1137-1142 10.1038/nbt.2401
54. Anderson, J. C., Voigt, C. A., and Arkin, A. P. (2007) Environmental signal integration by a modular AND gate Mol. Syst. Biol. 3, 133 10.1038/msb4100173
55. Saïda, F., Uzan, M., Odaert, B., and Bontems, F. (2006) Expression of highly toxic genes in E. coli: special strategies and genetic tools Curr. Protein Pept. Sci. 7, 47-56 10.2174/138920306775474095
56. Zerbib, D., Gamas, P., Chandler, M., Prentki, P., Bass, S., and Galas, D. (1985) Specificity of insertion of IS1 J. Mol. Biol. 185, 517-524 10.1016/0022-2836(85)90068-3
57. Stanton, B. C., Nielsen, A. A. K., Tamsir, A., Clancy, K., Peterson, T., and Voigt, C. A. (2014) Genomic mining of prokaryotic repressors for orthogonal logic gates Nat. Chem. Biol. 10, 99-105 10.1038/nchembio.1411
58. Tamsir, A., Tabor, J. J., and Voigt, C. A. (2011) Robust multicellular computing using genetically encoded NOR gates and chemical wires. Nature 469, 212-215 10.1038/nature09565
59. Anderson, J. C. (2009) Registry of Standard Biological Parts, www.partsregistry.org.
60. Buchler, N. E. and Cross, F. R. (2009) Protein sequestration generates a flexible ultrasensitive response in a genetic network Mol. Syst. Biol. 5, 272 10.1038/msb.2009.30
61. Lee, T. H. and Maheshri, N. (2012) A regulatory role for repeated decoy transcription factor binding sites in target gene expression Mol. Syst. Biol. 8, 576 10.1038/msb.2012.7
62. Rhodius, V. A., Segall-Shapiro, T. H., Sharon, B. D., Ghodasara, A., Orlova, E., Tabakh, H., Burkhardt, D. H., Clancy, K., Peterson, T. C., Gross, C. A., and Voigt, C. A. (2013) Design of orthogonal genetic switches based on a crosstalk map of σs, anti-σs, and promoters Mol. Syst. Biol. 9, 702 10.1038/msb.2013.58
63. 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 10.1186/1754-1611-4-12
64. Chen, Y.-J., Liu, P., Nielsen, A. A. K., Brophy, J. A. N., Clancy, K., Peterson, T., and Voigt, C. A. (2013) Characterization of 582 natural and synthetic terminators and quantification of their design constraints Nat. Methods 10, 659-664 10.1038/nmeth.2515
65. Canton, B., Labno, A., and Endy, D. (2008) Refinement and standardization of synthetic biological parts and devices Nat. Biotechnol. 26, 787-793 10.1038/nbt1413
66. Chalmers, R., Sewitz, S., Lipkow, K., and Crellin, P. (2000) Complete nucleotide sequence of Tn10 J. Bacteriol. 182, 2970-2972 10.1128/JB.182.10.2970-2972.2000
67. Liu, J. D. and Parkinson, J. S. (1989) Genetics and sequence analysis of the pcnB locus, an Escherichia coli gene involved in plasmid copy number control J. Bacteriol. 171, 1254-1261
68. Lopilato, J., Bortner, S., and Beckwith, J. (1986) Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB, reduce plasmid copy number of pBR322 and its derivatives Mol. Gen. Genet. MGG 205, 285-290 10.1007/BF00430440
69. Masters, M., Colloms, M. D., Oliver, I. R., He, L., Macnaughton, E. J., and Charters, Y. (1993) The pcnB gene of Escherichia coli, which is required for ColE1 copy number maintenance, is dispensable J. Bacteriol. 175, 4405-4413
70. Foster, T. J., Davis, M. A., Roberts, D. E., Takeshita, K., and Kleckner, N. (1981) Genetic organization of transposon Tn10 Cell 23, 201-213 10.1016/0092-8674(81)90285-3
71. Shearwin, K. E., Callen, B. P., and Egan, J. B. (2005) Transcriptional interference-a crash course Trends Genet. 21, 339-345 10.1016/j.tig.2005.04.009
72. Ghosal, D., Sommer, H., and Saedler, H. (1979) Nucleotide sequence of the transposable DNA-element IS2 Nucleic Acids Res. 6, 1111-1122 10.1093/nar/6.3.1111
73. Golby, P., Davies, S., Kelly, D. J., Guest, J. R., and Andrews, S. C. (1999) Identification and characterization of a two-component sensor-kinase and response-regulator system (DcuS-DcuR) controlling gene expression in response to C4-dicarboxylates in Escherichia coli J. Bacteriol. 181, 1238-1248
74. 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 10.1038/nature08480
75. Khan, A. I., Dinh, D. M., Schneider, D., Lenski, R. E., and Cooper, T. F. (2011) Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population Science 332, 1193-1196 10.1126/science.1203801
76. Eichenbaum, Z. and Livneh, Z. (1998) UV light induces IS10 transposition in Escherichia coli Genetics 149, 1173-1181
77. Twiss, E., Coros, A. M., Tavakoli, N. P., and Derbyshire, K. M. (2005) Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress Mol. Microbiol. 57, 1593-1607 10.1111/j.1365-2958.2005.04794.x
78. Sleight, S. C., Orlic, C., Schneider, D., and Lenski, R. E. (2008) Genetic Basis of Evolutionary Adaptation by Escherichia coli to Stressful Cycles of Freezing, Thawing and Growth Genetics 180, 431-443 10.1534/genetics.108.091330
79. Gonçalves, G. A. L., Oliveira, P. H., Gomes, A. G., Prather, K. L. J., Lewis, L. A., Prazeres, D. M. F., and Monteiro, G. A. (2014) Evidence that the insertion events of IS2 transposition are biased towards abrupt compositional shifts in target DNA and modulated by a diverse set of culture parameters Appl. Microbiol. Biotechnol. 98, 6609-6619 10.1007/s00253-014-5695-6
80. Gardner, T. S., Cantor, C. R., and Collins, J. J. (2000) Construction of a genetic toggle switch in Escherichia coli Nature 403, 339-342 10.1038/35002131
81. Kotula, J. W., Kerns, S. J., Shaket, L. A., Siraj, L., Collins, J. J., Way, J. C., and Silver, P. A. (2014) Programmable bacteria detect and record an environmental signal in the mammalian gut Proc. Natl. Acad. Sci. U. S. A. 111, 4838-4843 10.1073/pnas.1321321111
82. Green, A. A., Silver, P. A., Collins, J. J., and Yin, P. (2014) Toehold Switches: De-Novo-Designed Regulators of Gene Expression Cell 159, 925-939 10.1016/j.cell.2014.10.002
83. Larson, M. H., Gilbert, L. A., Wang, X., Lim, W. A., Weissman, J. S., and Qi, L. S. (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression Nat. Protoc. 8, 2180-2196 10.1038/nprot.2013.132
84. Bikard, D., Jiang, W., Samai, P., Hochschild, A., Zhang, F., and Marraffini, L. A. (2013) Programmable repression and activation of bacterial gene expression using an engineered CRISPR-Cas system Nucleic Acids Res. 41, 7429-7437 10.1093/nar/gkt520
85. Tabor, J. J., Salis, H., Simpson, Z. B., Chevalier, A. A., Levskaya, A., Marcotte, E. M., Voigt, C. A., and Ellington, A. D. (2009) A Synthetic Genetic Edge Detection Program Cell 137, 1272-1281 10.1016/j.cell.2009.04.048
86. Caliando, B. J. and Voigt, C. A. (2015) Targeted DNA degradation using a CRISPR device stably carried in the host genome Nat. Commun. 6, 6989 10.1038/ncomms7989
87. Lajoie, M. J., Rovner, A. J., Goodman, D. B., Aerni, H.-R., Haimovich, A. D., Kuznetsov, G., Mercer, J. A., Wang, H. H., Carr, P. A., Mosberg, J. A., Rohland, N., Schultz, P. G., Jacobson, J. M., Rinehart, J., Church, G. M., and Isaacs, F. J. (2013) Genomically Recoded Organisms Expand Biological Functions Science 342, 357-360 10.1126/science.1241459
88. Isaacs, F. J., Carr, P. A., Wang, H. H., Lajoie, M. J., Sterling, B., Kraal, L., Tolonen, A. C., Gianoulis, T. A., Goodman, D. B., Reppas, N. B., Emig, C. J., Bang, D., Hwang, S. J., Jewett, M. C., Jacobson, J. M., and Church, G. M. (2011) Precise Manipulation of Chromosomes in Vivo Enables Genome-Wide Codon Replacement Science 333, 348-353 10.1126/science.1205822
89. Elowitz, M. B. and Leibler, S. (2000) A synthetic oscillatory network of transcriptional regulators Nature 403, 335-338 10.1038/35002125
90. Cambray, G., Guimaraes, J. C., Mutalik, V. K., Lam, C., Mai, Q.-A., Thimmaiah, T., Carothers, J. M., Arkin, A. P., and Endy, D. (2013) Measurement and modeling of intrinsic transcription terminators Nucleic Acids Res. 41, 5139-5148 10.1093/nar/gkt163
91. Mutalik, V. K., Guimaraes, J. C., Cambray, G., Lam, C., Christoffersen, M. J., Mai, Q.-A., Tran, A. B., Paull, M., Keasling, J. D., Arkin, A. P., and Endy, D. (2013) Precise and reliable gene expression via standard transcription and translation initiation elements Nat. Methods 10, 354-360 10.1038/nmeth.2404
92. Stoebel, D. M., Hokamp, K., Last, M. S., and Dorman, C. J. (2009) Compensatory evolution of gene regulation in response to stress by Escherichia coli lacking RpoS PLoS Genet. 5, e1000671 10.1371/journal.pgen.1000671
93. Glick, B. R. (1995) Metabolic load and heterologous gene expression Biotechnol. Adv. 13, 247-261 10.1016/0734-9750(95)00004-A
94. 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 10.1126/science.1192588
95. Sleight, S. C. and Sauro, H. M. (2013) Visualization of Evolutionary Stability Dynamics and Competitive Fitness of Escherichia coli Engineered with Randomized Multigene Circuits ACS Synth. Biol. 2, 519-528 10.1021/sb400055h
96. Bienick, M. S., Young, K. W., Klesmith, J. R., Detwiler, E. E., Tomek, K. J., and Whitehead, T. A. (2014) The Interrelationship between Promoter Strength, Gene Expression, and Growth Rate PLoS One 9, e109105 10.1371/journal.pone.0109105
97. Gregg, C. J., Lajoie, M. J., Napolitano, M. G., Mosberg, J. A., Goodman, D. B., Aach, J., Isaacs, F. J., and Church, G. M. (2014) Rational optimization of tolC as a powerful dual selectable marker for genome engineering Nucleic Acids Res. 42, 4779-4790 10.1093/nar/gkt1374
98. 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 10.1186/1475-2859-11-11
99. 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 10.1186/1475-2859-9-38
100. Darmon, E. and Leach, D. R. F. (2014) Bacterial Genome Instability Microbiol. Mol. Biol. Rev. 78, 1-39 10.1128/MMBR.00035-13
101. Foster, P. L. (2007) Stress-Induced Mutagenesis in Bacteria Crit. Rev. Biochem. Mol. Biol. 42, 373-397 10.1080/10409230701648494
102. 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 10.1038/nature08187
103. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., and Zhang, F. (2013) Multiplex Genome Engineering Using CRISPR/Cas Systems Science 339, 819-823 10.1126/science.1231143
104. Pijkeren, J. P. v. and Britton, R. A. (2014) Precision genome engineering in lactic acid bacteria Microb. Cell Fact. 13, S10 10.1186/1475-2859-13-S1-S10
105. Dalia, A. B., McDonough, E., and Camilli, A. (2014) Multiplex genome editing by natural transformation Proc. Natl. Acad. Sci. U. S. A. 111, 8937-8942 10.1073/pnas.1406478111
106. Du, D., Wang, L., Tian, Y., Liu, H., Tan, H., and Niu, G. (2015) Genome engineering and direct cloning of antibiotic gene clusters via phage ΦBT1 integrase-mediated site-specific recombination in Streptomyces Sci. Rep. 5, 8740 10.1038/srep08740
107. Galdzicki, M., Clancy, K. P., Oberortner, E., Pocock, M., Quinn, J. Y., Rodriguez, C. A., Roehner, N., Wilson, M. L., Adam, L., Anderson, J. C., Bartley, B. A., Beal, J., Chandran, D., Chen, J., Densmore, D., Endy, D., Grünberg, R., Hallinan, J., Hillson, N. J., Johnson, J. D., Kuchinsky, A., Lux, M., Misirli, G., Peccoud, J., Plahar, H. A., Sirin, E., Stan, G.-B., Villalobos, A., Wipat, A., Gennari, J. H., Myers, C. J., and Sauro, H. M. (2014) The Synthetic Biology Open Language (SBOL) provides a community standard for communicating designs in synthetic biology Nat. Biotechnol. 32, 545-550 10.1038/nbt.2891
108. Jasiecki, J. and Wegrzyn, G. (2006) Transcription start sites in the promoter region of the Escherichia coli pcnB (plasmid copy number) gene coding for poly(A) polymerase I Plasmid 55, 169-172 10.1016/j.plasmid.2005.10.002
109. 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 10.1016/j.jbiotec.2005.11.014
110. So, L., Ghosh, A., Zong, C., Sepúlveda, L. A., Segev, R., and Golding, I. (2011) General properties of transcriptional time series in Escherichia coli Nat. Genet. 43, 554-560 10.1038/ng.821
111. Bernstein, J. A., Khodursky, A. B., Lin, P.-H., Lin-Chao, S., and Cohen, S. N. (2002) Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays Proc. Natl. Acad. Sci. U. S. A. 99, 9697-9702 10.1073/pnas.112318199