A sigma factor toolbox for orthogonal gene expression in Escherichia coli

Nucleic Acids Research

Volumn 46, Issue 4, 2018, Pages 2133-2144

  Bervoets, Indra ^a   Van Brempt, Maarten ^b   Van Nerom, Katleen ^a   Van Hove, Bob ^b   Maertens, Jo ^b   De Mey, Marjan ^b   Charlier, Daniel ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

SIGMA FACTOR;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENOME; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE LIBRARY; GENE SEQUENCE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM;

BACILLUS SUBTILIS; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENOME; PLASMIDS; PROMOTER REGIONS, GENETIC; SIGMA FACTOR;

EID: 85043300053     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gky010     Document Type: Article

References (76)

1. Wargacki, A.J., Leonard, E., Win, M.N., Regitsky, D.D., Santos, C.N.S., Kim, P.B., Cooper, S.R., Raisner, R.M., Herman, A., Sivitz, A.B. et al. (2012) An engineered microbial platform for direct biofuel production from brown macroalgae. Science, 335, 308-313.
2. Cheon, S., Kim, H.M., Gustavsson, M. and Lee, S.Y. (2016) Recent trends in metabolic engineering of microorganisms for the production of advanced biofuels. Curr. Opin. Chem. Biol., 35, 10-21.
3. Pandey, R.P., Parajuli, P., Koffas, M.A.G. and Sohng, J.K. (2016) Microbial production of natural and non-natural flavonoids: Pathway engineering, directed evolution and systems/synthetic biology. Biotechnol. Adv., 34, 634-662.
4. Paddon, C.J. and Keasling, J.D. (2014) Semi-synthetic artemisinin: A model for the use of synthetic biology in pharmaceutical development. Nat. Rev. Microbiol., 12, 355-367.
5. Trantas, E.A., Koffas, M.A.G., Xu, P. and Ververidis, F. (2015) When plants produce not enough or at all: Metabolic engineering of flavonoids in microbial hosts. Front. Plant Sci., 6, 7.
6. Keasling, J.D. (2010) Manufacturing molecules through metabolic engineering. Science, 330, 1355-1358.
7. Woolston, B.M., Edgar, S. and Stephanopoulos, G. (2013) Metabolic engineering: Past and future. Annu. Rev. Chem. Biomol. Eng., 4, 259-288.
8. Singh, A., Cher Soh, K., Hatzimanikatis, V. and Gill, R.T. (2011) Manipulating redox and ATP balancing for improved production of succinate in E. coli. Metab. Eng., 13, 76-81.
9. Tai, M. and Stephanopoulos, G. (2013) Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab. Eng., 15, 1-9.
10. Arense, P., Bernal, V., Charlier, D., Iborra, J.L., Foulquié-Moreno, M.R. and Cánovas, M. (2013) Metabolic engineering for high yielding L(-)-carnitine production in Escherichia coli. Microb. Cell Fact., 12, 56.
11. 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. et al. (2013) Precise and reliable gene expression via standard transcription and translation initiation elements. Nat. Methods, 10, 354-360.
12. Davis, J.H., Rubin, A.J. and Sauer, R.T. (2011) Design, construction and characterization of a set of insulated bacterial promoters. Nucleic Acids Res., 39, 1131-1141.
13. De Mey, M., Maertens, J., Lequeux, G.J., Soetaert, W.K. and Vandamme, E.J. (2007) Construction and model-based analysis of a promoter library for E. coli: An indispensable tool for metabolic engineering. BMC Biotechnol., 7, 34.
14. Trubitsyna, M., Michlewski, G., Cai, Y., Elfick, A. and French, C.E. (2014) PaperClip: Rapid multi-part DNA assembly from existing libraries. Nucleic Acids Res., 42, e154.
15. Coussement, P., Maertens, J., Beauprez, J., Van Bellegem, W. and De Mey, M. (2014) One step DNA assembly for combinatorial metabolid engineering. Metab. Eng., 23, 70-77.
16. Quan, J. and Tian, J. (2009) Circular polymerase extension cloning of complex gene libraries and pathways. PLoS One, 4, e6441.
17. Zhang, Y., Werling, U. and Edelmann, W. (2012) SLiCE: A novel bacterial cell extract-based DNA cloning method. Nucleic Acids Res., 40, e55.
18. Werner, S., Engler, C., Weber, E., Gruetzner, R. and Marillonnet, S. (2012) Fast track assembly of multigene constructs using golden gate cloning and the MoClo system. Biobugs, 3, 38-43.
19. Van Hove, B., Guidi, C., De Wannemaeker, L., Maertens, J. and De Mey, M. (2017) Recursive DNA assembly using protected oligonucleotide duplex assisted cloning (PODAC). ACS Synth. Biol., 6, 943-949.
20. De Mey, M., Maertens, J., Boogmans, S., Soetaert, W.K., Vandamme, E.J., Cunin, R. and Foulquié-Moreno, M.R. (2010) Promoter knock-in: A novel rational method for the fine tuning of genes. BMC Biotechnol., 10, 26.
21. Zou, R., Zhou, K., Stephanopoulos, G. and Too, H.P. (2013) Combinatorial engineering of 1-Deoxy-D-Xylulose 5-Phosphate pathway using cross-lapping in vitro assembly (CLIVA) method. PLoS OnE, 8, e79557.
22. De Paepe, B., Peters, G., Coussement, P., Maertens, J. and De Mey, M. (2017) Tailor-made transcriptional biosensors for optimizing microbial cell factories. J. Ind. Microbiol. Biotechnol., 44, 623-645.
23. Wu, G., Yan, Q., Jones, J.A., Tang, Y.J., Fong, S.S. and Koffas, M.A.G. (2016) Metabolic burden: Cornerstones in synthetic biology and metabolic engineering applications. Trends Biotechnol., 34, 652-664.
24. Bradley, R.W., Buck, M. and Wang, B. (2016) Tools and principles for microbial gene circuit engineering. J. Mol. Biol., 428, 862-888.
25. Slusarczyk, A.L., Lin, A. and Weiss, R. (2012) Foundations for the design and implementation of synthetic genetic circuits. Nat. Rev. Genet., 13, 406-420.
26. An, W. and Chin, J.W. (2009) Synthesis of orthogonal transcription-translation networks. Proc. Natl. Acad. Sci. U.S.A., 106, 8477-8482.
27. Salis, H.M., Mirsky, E.A. and Voigt, C.A. (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat. Biotechnol., 27, 946-950.
28. Li, G.-W., Oh, E. and Weissman, J.S. (2012) The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature, 484, 538-541.
29. Sharma, V., Nomura, Y. and Yokobayashi, Y. (2008) Engineering complex riboswitch regulation by dual genetic selection. J. Am. Chem. Soc., 130, 16310-16315.
30. Na, D., Yoo, S.M., Chung, H., Park, H., Park, J.H. and Lee, S.Y. (2013) Metabolic engineering of Escherichia coli using synthetic small regulatory RNAs. Nat. Biotechnol., 31, 170-174.
31. 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.
32. 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.
33. Stanton, B.C., Nielsen, A.A.K., Tamsir, A., Clancy, K., Peterson, T. and Voigt, C.A. (2013) Genomic mining of prokaryotic repressors for orthogonal logic gates. Nat. Chem. Biol., 10, 99-105.
34. 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.
35. Brewster, R.C., Jones, D.L. and Phillips, R. (2012) Tuning promoter strength through RNA polymerase binding site design in Escherichia coli. PLoS Comput. Biol., 8, e1002811.
36. Temme, K., Hill, R., Segall-Shapiro, T.H., Moser, F. and Voigt, C.A. (2012) Modular control of multiple pathways using engineered orthogonal T7 polymerases. Nucleic Acids Res., 40, 8773-8781.
37. Meyer, A.J., Ellefson, J.W. and Ellington, A.D. (2015) Directed evolution of a panel of orthogonal T7 RNA polymerase variants for in vivo or in vitro synthetic circuitry. ACS Synth. Biol., 4, 1070-1076.
38. Shis, D.L. and Bennett, M.R. (2013) Library of synthetic transcriptional AND gates built with split T7 RNA polymerase mutants. Proc. Natl. Acad. Sci. U.S.A., 110, 5028-5033.
39. Segall-Shapiro, T.H., Meyer, A.J., Ellington, A.D., Sontag, E.D. and Voigt, C.A. (2014) A 'resource allocator' for transcription based on a highly fragmented T7 RNA polymerase. Mol. Syst. Biol., 10, 742.
40. Jones, J.A., Vernacchio, V.R., Lachance, D.M., Lebovich, M., Fu, L., Shirke, A.N., Schultz, V.L., Cress, B., Linhardt, R.J. and Koffas, M.A.G. (2015) ePathOptimize: A combinatorial approach for transcriptional balancing of metabolic pathways. Sci. Rep., 5, 11301.
41. 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. et al. (2013) Design of orthogonal genetic switches based on a crosstalk map of-s, anti-s, and promoters. Mol. Syst. Biol., 9, 702-713.
42. Paget, M. (2015) Bacterial sigma factors and anti-sigma factors: Structure, function and distribution. Biomolecules, 5, 1245-1265.
43. Kazmierczak, M.J., Wiedmann, M. and Boor, K.J. (2005) Alternative sigma factors and their roles in bacterial virulence. Microbiol. Mol. Biol. Rev., 69, 527-543.
44. Gruber, T.M. and Gross, C.A. (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol., 57, 441-466.
45. 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.
46. Dagert, M. and Ehrlich, S.D. (1979) Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene, 6, 23-28.
47. Kahm, M., Hasenbrink, G., Lichtenberg-Frate, H., Ludwig, J. and kschischo, M. (2010) Grofit: Fitting biological growth curves with R. J. Stat. Softw., 33, 7.
48. Hengge-Aronis, R. (2002) Stationary phase gene regulation: What makes an Escherichia coli promoter sigmaS-selective? Curr. Opin. Microbiol., 5, 591-595.
49. Lonetto, M., Gribskov, M. and Gross, C.A. (1992) The sigma 70 family: Sequence conservation and evolutionary relationships. J. Bacteriol., 174, 3843-3849.
50. Chen, Y.F. and Helmann, J.D. (1992) Restoration of motility to an Escherichia coli fliA flagellar mutant by a Bacillus subtilis sigma factor. Proc. Natl. Acad. Sci. U.S.A., 89, 5123-5127.
51. Errington, J. (2003) Regulation of endospore formation in Bacillus subtilis. Nat. Rev. Microbiol., 1, 117-126.
52. Piggot, P.J. and Hilbert, D.W. (2004) Sporulation of Bacillus subtilis. Curr. Opin. Microbiol., 7, 579-586.
53. Maeda, H., Fujita, N. and Ishihama, A. (2000) Competition among seven Escherichia coli sigma subunits: Relative binding affinities to the core RNA polymerase. Nucleic Acids Res., 28, 3497-3503.
54. Mitchell, J.E., Zheng, D., Busby, S.J.W. and Minchin, S.D. (2003) Identification and analysis of 'extended-10' promoters in Escherichia coli. Nucleic Acids Res., 31, 4689-4695.
55. Grigorova, I.L., Phleger, N.J., Mutalik, V.K. and Gross, C.A. (2006) Insights into transcriptional regulation and sigma competition from an equilibrium model of RNA polymerase binding to DNA. Proc. Natl. Acad. Sci. U.S.A., 103, 5332-5337.
56. Petersohn, A., Bernhardt, J., Gerth, U., Hoper, D., Koburger, T., Volker, U. and Hecker, M. (1999) Identification of sigma(B)-dependent genes in Bacillus subtilis using a promoter consensus-directed search and oligonucleotide hybridization. J. Bacteriol., 181, 5718-5724.
57. Amaya, E., Khvorova, A. and Piggot, P.J. (2001) Analysis of promoter recognition in vivo directed by F of Bacillus subtilis by using random-sequence oligonucleotides. J. Bacteriol., 183, 3623-3630.
58. Wang, S.T., Setlow, B., Conlon, E.M., Lyon, J.L., Imamura, D., Sato, T., Setlow, P., Losick, R. and Eichenberger, P. (2006) The forespore line of gene expression in Bacillus subtilis. J. Mol. Biol., 358, 16-37.
59. Britton, R.A., Eichenberger, P., Gonzalez-Pastor, J.E., Fawcett, P., Monson, R., Losick, R. and Grossman, A.D. (2002) Genome-wide analysis of the stationary-phase sigma factor (Sigma-H) regulon of Bacillus subtilis. J. Bacteriol., 184, 4881-4890.
60. Eiamphungporn, W. and Helmann, J.D. (2008) The Bacillus subtilis-M regulon and its contribution to cell envelope stress responses. Mol. Microbiol., 67, 830-848.
61. Cao, M., Kobel, P.A., Morshedi, M.M., Wu, M.F.W., Paddon, C. and Helmann, J.D. (2002) Defining the Bacillus subtilis-W regulon: A comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J. Mol. Biol., 316, 443-457.
62. Cao, M. and Helmann, J.D. (2004) The Bacillus subtilis extracytoplasmic-function X factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J. Bacteriol., 186, 1136-1146.
63. Tyo, K.E.J., Ajikumar, P.K. and Stephanopoulos, G. (2009) Stabilized gene duplication enables long-term selection-free heterologous pathway expression. Nat. Biotechnol., 27, 760-765.
64. Shimada, T., Tanaka, K. and Ishihama, A. (2017) The whole set of the constitutive promoters recognized by four minor sigma subunits of Escherichia coli RNA polymerase. PLoS One, 12, e0179181.
65. Lucks, J.B., Qi, L., Whitaker, W.R. and Arkin, A.P. (2008) Toward scalable parts families for predictable design of biological circuits. Curr. Opin. Microbiol., 11, 567-573.
66. Browning, D.F. and Busby, S.J.W. (2004) The regulation of bacterial transcription initiation. Nat. Rev. Microbiol., 2, 57-65.
67. Sun, D., Fajardo-Cavazos, P., Sussman, M.D., Tovar-Rojo, F., Cabrera-Martinez, R.M. and Setlow, P. (1991) Effect of chromosome location of Bacillus subtilis forespore genes on their spo gene dependence and transcription by E sigma F: Identification of features of good E sigma F-dependent promoters. J. Bacteriol., 173, 7867-7874.
68. Bagyan, I., Casillas-Martinez, L. and Setlow, P. (1998) The katX gene, which codes for the catalase in spores of Bacillus subtilis, is a forespore-specific gene controlled by sigmaF, and KatX is essential for hydrogen peroxide resistance of the germinating spore. J. Bacteriol., 180, 2057-2062.
69. Paddon, C.J., Westfall, P.J., Pitera, D.J., Benjamin, K., Fisher, K., McPhee, D., Leavell, M.D., Tai, A., Main, A., Eng, D. et al. (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature, 496, 528-532.
70. Jullesson, D., David, F., Pfleger, B. and Nielsen, J. (2015) Impact of synthetic biology and metabolic engineering on industrial production of fine chemicals. Biotechnol. Adv., 33, 1395-1402.
71. Ajikumar, P.K., Xiao, W.H., Tyo, K.E.J., Wang, Y., Simeon, F., Leonard, E., Mucha, O., Phon, T.H., Pfeifer, B. and Stephanopoulos, G. (2010) Isoprenoid pathway optimization for taxol precursor overproduction in Escherichia coli. Science, 330, 70-74.
72. Xu, P., Gu, Q., Wang, W., Wong, L., Bower, A.G.W., Collins, C.H. and Koffas, M.A.G. (2013) Modular optimization of multi-gene pathways for fatty acids production in E. coli. Nat. Commun., 4, 1409.
73. Gu, L., Zhang, J., Du, G. and Chen, J. (2015) Multivariate modular engineering of the protein secretory pathway for production of heterologous glucose oxidase in Pichia pastoris. Enzyme Microb. Technol., 68, 33-42.
74. Jones, J.A., Toparlak, O .D. and Koffas, M.A. (2015) Metabolic pathway balancing and its role in the production of biofuels and chemicals. Curr. Opin. Biotechnol., 33, 52-59.
75. Wu, J., Liu, P., Fan, Y., Bao, H., Du, G., Zhou, J. and Chen, J. (2013) Multivariate modular metabolic engineering of Escherichia coli to produce resveratrol from L-tyrosine. J. Biotechnol., 167, 404-411.
76. Qiu, J. and Helmann, J.D. (2001) The-10 region is a key promoter specificity determinant for the Bacillus subtilis extracytoplasmic-function sigma factors sigma(X) and sigma(W). J. Bacteriol., 183, 1921-1927.