Deconvolution of Gene Expression Noise into Spatial Dynamics of Transcription Factor-Promoter Interplay

ACS Synthetic Biology

Volumn 6, Issue 7, 2017, Pages 1359-1369

  Goñi Moreno, Ángel ^a,b   Benedetti, Ilaria ^a   Kim, Juhyun ^a   De Lorenzo, Víctor ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

bet hedging; intracellular heterogeneity; Pseudomonas putida; TOL plasmid; transcriptional noise

Indexed keywords

TRANSCRIPTION FACTOR; BACTERIAL PROTEIN;

ARTICLE; FLOW CYTOMETRY; GENE EXPRESSION; MATHEMATICAL MODEL; NOISE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOMONAS PUTIDA; SIMULATION; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; GENETICS; PHYSIOLOGY; PLASMID;

BACTERIAL PROTEINS; COMPUTER SIMULATION; GENE EXPRESSION REGULATION, BACTERIAL; PLASMIDS; PROMOTER REGIONS, GENETIC; PSEUDOMONAS PUTIDA; TRANSCRIPTION FACTORS;

EID: 85025162142     PISSN: None     EISSN: 21615063     Source Type: Journal    
DOI: 10.1021/acssynbio.6b00397     Document Type: Article

References (83)

1. Kærn, M., Elston, T. C., Blake, W. J., and Collins, J. J. (2005) Stochasticity in gene expression: from theories to phenotypes Nat. Rev. Genet. 6, 451-464 10.1038/nrg1615
2. Golding, I., Paulsson, J., Zawilski, S. M., and Cox, E. C. (2005) Real-time kinetics of gene activity in individual bacteria Cell 123, 1025-1036 10.1016/j.cell.2005.09.031
3. Raj, A. and van Oudenaarden, A. (2008) Nature, nurture, or chance: stochastic gene expression and its consequences Cell 135, 216-226 10.1016/j.cell.2008.09.050
4. Eldar, A. and Elowitz, M. B. (2010) Functional roles for noise in genetic circuits Nature 467, 167-173 10.1038/nature09326
5. Rinott, R., Jaimovich, A., and Friedman, N. (2011) Exploring transcription regulation through cell-to-cell variability Proc. Natl. Acad. Sci. U. S. A. 108, 6329-6334 10.1073/pnas.1013148108
6. McAdams, H. H. and Arkin, A. (1999) It'sa noisy business! Genetic regulation at the nanomolar scale Trends Genet. 15, 65-69 10.1016/S0168-9525(98)01659-X
7. Hansen, A. S. and O'Shea, E. K. (2013) Promoter decoding of transcription factor dynamics involves a trade-off between noise and control of gene expression Mol. Syst. Biol. 9, 704 10.1038/msb.2013.56
8. Munsky, B., Neuert, G., and van Oudenaarden, A. (2012) Using gene expression noise to understand gene regulation Science 336, 183-187 10.1126/science.1216379
9. Purvis, J. E. and Lahav, G. (2013) Encoding and decoding cellular information through signaling dynamics Cell 152, 945-956 10.1016/j.cell.2013.02.005
10. Brehm-Stecher, B. F. and Johnson, E. A. (2004) Single-cell microbiology: tools, technologies, and applications Microbiology and molecular biology reviews 68, 538-559 10.1128/MMBR.68.3.538-559.2004
11. Czechowska, K., Johnson, D. R., and van der Meer, J. R. (2008) Use of flow cytometric methods for single-cell analysis in environmental microbiology Curr. Opin. Microbiol. 11, 205-212 10.1016/j.mib.2008.04.006
12. Kortmann, H., Blank, L. M., and Schmid, A. (2010) Single cell analytics: An overview, In High Resolution Microbial Single Cell Analytics, pp 99-122, Springer.
13. Taniguchi, Y., Choi, P. J., Li, G.-W., Chen, H., Babu, M., Hearn, J., Emili, A., and Xie, X. S. (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells Science 329, 533-538 10.1126/science.1188308
14. Zong, C., So, L. h., Sepúlveda, L. A., Skinner, S. O., and Golding, I. (2010) Lysogen stability is determined by the frequency of activity bursts from the fate-determining gene Mol. Syst. Biol. 6, 440 10.1038/msb.2010.96
15. Chong, S., Chen, C., Ge, H., and Xie, X. S. (2014) Mechanism of transcriptional bursting in bacteria Cell 158, 314-326 10.1016/j.cell.2014.05.038
16. So, L.-h., 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
17. Nikel, P. I., Silva-Rocha, R., Benedetti, I., and Lorenzo, V. (2014) The private life of environmental bacteria: pollutant biodegradation at the single cell level Environ. Microbiol. 16, 628-642 10.1111/1462-2920.12360
18. Nikel, P. I., Martínez-García, E., and de Lorenzo, V. (2014) Biotechnological domestication of pseudomonads using synthetic biology Nat. Rev. Microbiol. 12, 368-379 10.1038/nrmicro3253
19. De Las Heras, A., Fraile, S., and de Lorenzo, V. (2012) Increasing signal specificity of the TOL network of Pseudomonas putida mt-2 by rewiring the connectivity of the master regulator XylR PLoS Genet. 8, e1002963 10.1371/journal.pgen.1002963
20. Nikel, P. I., Romero-Campero, F. J., Zeidman, J. A., Goñi-Moreno, á., and de Lorenzo, V. (2015) The glycerol-dependent metabolic persistence of Pseudomonas putida KT2440 reflects the regulatory logic of the GlpR repressor mBio 6, e00340-00315 10.1128/mBio.00340-15
21. Silva-Rocha, R., Pérez-Pantoja, D., and de Lorenzo, V. (2013) Decoding the genetic networks of environmental bacteria: regulatory moonlighting of the TOL system of Pseudomonas putida mt-2 ISME J. 7, 229 10.1038/ismej.2012.98
22. Ramos, J. L., Marqués, S., and Timmis, K. N. (1997) Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators Annu. Rev. Microbiol. 51, 341-373 10.1146/annurev.micro.51.1.341
23. González-Pérez, M., Marqués, S., Domínguez-Cuevas, P., and Ramos, J. L. (2002) XylS activator and RNA polymerase binding sites at the Pm promoter overlap FEBS Lett. 519, 117-122 10.1016/S0014-5793(02)02730-8
24. Pérez-Pantoja, D., Kim, J., Silva-Rocha, R., and Lorenzo, V. (2015) The differential response of the Pben promoter of Pseudomonas putida mt-2 to BenR and XylS prevents metabolic conflicts in m-xylene biodegradation Environ. Microbiol. 17, 64-75 10.1111/1462-2920.12443
25. González-Pérez, M. M., Ramos, J. L., and Marqués, S. (2004) Cellular XylS levels are a function of transcription of xylS from two independent promoters and the differential efficiency of translation of the two mRNAs Journal of bacteriology 186, 1898-1901 10.1128/JB.186.6.1898-1901.2003
26. Goñi-Moreno, A. (2014) On genetic logic circuits: forcing digital electronics standards? Memetic Computing 6, 149-155 10.1007/s12293-014-0136-8
27. Dublanche, Y., Michalodimitrakis, K., Kümmerer, N., Foglierini, M., and Serrano, L. (2006) Noise in transcription negative feedback loops: simulation and experimental analysis Mol. Syst. Biol. 2, 41 10.1038/msb4100081
28. Goñi-Moreno, A. and Amos, M. (2012) Continuous computation in engineered gene circuits BioSystems 109, 52-56 10.1016/j.biosystems.2012.02.001
29. Balagaddé, F. K., Song, H., Ozaki, J., Collins, C. H., Barnet, M., Arnold, F. H., Quake, S. R., and You, L. (2008) A synthetic Escherichia coli predator-prey ecosystem Mol. Syst. Biol. 4, 187 10.1038/msb.2008.24
30. Andersen, J. B., Sternberg, C., Poulsen, L. K., Bjørn, S. P., Givskov, M., and Molin, S. (1998) New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria Appl. Environ. Microbiol. 64, 2240-2246
31. de-Leon, S. B.-T. and Davidson, E. H. (2009) Modeling the dynamics of transcriptional gene regulatory networks for animal development Dev. Biol. 325, 317-328 10.1016/j.ydbio.2008.10.043
32. Velázquez, F., Parro, V., and de Lorenzo, V. (2005) Inferring the genetic network of m-xylene metabolism through expression profiling of the xyl genes of Pseudomonas putida mt-2 Mol. Microbiol. 57, 1557-1569 10.1111/j.1365-2958.2005.04787.x
33. Elf, J., Li, G.-W., and Xie, X. S. (2007) Probing transcription factor dynamics at the single-molecule level in a living cell Science 316, 1191-1194 10.1126/science.1141967
34. Miró-Bueno, J. M. and Rodríguez-Patón, A. (2011) A simple negative interaction in the positive transcriptional feedback of a single gene is sufficient to produce reliable oscillations PLoS One 6, e27414 10.1371/journal.pone.0027414
35. Moon, T. S., Lou, C., Tamsir, A., Stanton, B. C., and Voigt, C. A. (2012) Genetic programs constructed from layered logic gates in single cells Nature 491, 249-253 10.1038/nature11516
36. Wang, B., Kitney, R. I., Joly, N., and Buck, M. (2011) Engineering modular and orthogonal genetic logic gates for robust digital-like synthetic biology Nat. Commun. 2, 508 10.1038/ncomms1516
37. 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
38. Murphy, K. F., Balázsi, G., and Collins, J. J. (2007) Combinatorial promoter design for engineering noisy gene expression Proc. Natl. Acad. Sci. U. S. A. 104, 12726-12731 10.1073/pnas.0608451104
39. Murphy, K. F., Adams, R. M., Wang, X., Balazsi, G., and Collins, J. J. (2010) Tuning and controlling gene expression noise in synthetic gene networks Nucleic Acids Res. 38, gkq091 10.1093/nar/gkq091
40. Goñi-Moreno, A. and Amos, M. (2012) A reconfigurable NAND/NOR genetic logic gate BMC Syst. Biol. 6, 126 10.1186/1752-0509-6-126
41. Daniel, R., Rubens, J. R., Sarpeshkar, R., and Lu, T. K. (2013) Synthetic analog computation in living cells Nature 497, 619-623 10.1038/nature12148
42. Miklos, A. C., Sarkar, M., Wang, Y., and Pielak, G. J. (2011) Protein crowding tunes protein stability J. Am. Chem. Soc. 133, 7116-7120 10.1021/ja200067p
43. Parry, B. R., Surovtsev, I. V., Cabeen, M. T., O'Hern, C. S., Dufresne, E. R., and Jacobs-Wagner, C. (2014) The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity Cell 156, 183-194 10.1016/j.cell.2013.11.028
44. Gahlmann, A. and Moerner, W. E. (2014) Exploring bacterial cell biology with single-molecule tracking and super-resolution imaging Nat. Rev. Microbiol. 12, 9-22 10.1038/nrmicro3154
45. Uphoff, S. and Kapanidis, A. N. (2014) Studying the organization of DNA repair by single-cell and single-molecule imaging DNA Repair 20, 32-40 10.1016/j.dnarep.2014.02.015
46. Uhlenbeck, G. E. and Ornstein, L. S. (1930) On the theory of the Brownian motion Phys. Rev. 36, 823 10.1103/PhysRev.36.823
47. Saffman, P. G. and Delbrück, M. (1975) Brownian motion in biological membranes Proc. Natl. Acad. Sci. U. S. A. 72, 3111-3113 10.1073/pnas.72.8.3111
48. Gowrishankar, J. and Harinarayanan, R. (2004) Why is transcription coupled to translation in bacteria? Mol. Microbiol. 54, 598-603 10.1111/j.1365-2958.2004.04289.x
49. Burmann, B. M., Schweimer, K., Luo, X., Wahl, M. C., Stitt, B. L., Gottesman, M. E., and Rösch, P. (2010) A NusE: NusG complex links transcription and translation Science 328, 501-504 10.1126/science.1184953
50. Miller, O. L., Hamkalo, B. A., and Thomas, C. A. (1970) Visualization of bacterial genes in action Science 169, 392-395 10.1126/science.169.3943.392
51. Balleza, E., Lopez-Bojorquez, L. N., Martínez-Antonio, A., Resendis-Antonio, O., Lozada-Chávez, I., Balderas-Martínez, Y. I., Encarnación, S., and Collado-Vides, J. (2009) Regulation by transcription factors in bacteria: beyond description FEMS microbiology reviews 33, 133-151 10.1111/j.1574-6976.2008.00145.x
52. Silva-Rocha, R., De Jong, H., Tamames, J., and De Lorenzo, V. (2011) The logic layout of the TOL network of Pseudomonas putida pWW0 plasmid stems from a metabolic amplifier motif (MAM) that optimizes biodegradation of m-xylene BMC Syst. Biol. 5, 191 10.1186/1752-0509-5-191
53. Weng, X. and Xiao, J. (2014) Spatial organization of transcription in bacterial cells Trends Genet. 30, 287-297 10.1016/j.tig.2014.04.008
54. Yu, I., Mori, T., Ando, T., Harada, R., Jung, J., Sugita, Y., and Feig, M. (2016) Biomolecular interactions modulate macromolecular structure and dynamics in atomistic model of a bacterial cytoplasm eLife 5, e19274 10.7554/eLife.19274
55. González-Pérez, M. M., Ramos, J. L., Gallegos, M. a.-T., and Marqués, S. (1999) Critical nucleotides in the upstream region of the XylS-dependent TOL meta-cleavage pathway operon promoter as deduced from analysis of mutants J. Biol. Chem. 274, 2286-2290 10.1074/jbc.274.4.2286
56. Halford, S. E. (2009) An end to 40 years of mistakes in DNA-protein association kinetics?, Portland Press Limited.
57. Ishihama, A., Kori, A., Koshio, E., Yamada, K., Maeda, H., Shimada, T., Makinoshima, H., Iwata, A., and Fujita, N. (2014) Intracellular concentrations of transcription factors in Escherichia coli: 65 species with known regulatory functions J. Bacteriol. 196, 01579-01514 10.1128/JB.01579-14
58. Dröge, P. and Müller-Hill, B. (2001) High local protein concentrations at promoters: strategies in prokaryotic and eukaryotic cells BioEssays 23, 179-183 10.1002/1521-1878(200102)23:2<179::AID-BIES1025>3.0.CO;2-6
59. Warren, P. B. and Ten Wolde, P. R. (2004) Statistical analysis of the spatial distribution of operons in the transcriptional regulation network of Escherichia coli J. Mol. Biol. 342, 1379-1390 10.1016/j.jmb.2004.07.074
60. van Zon, J. S., Morelli, M. J., Tǎnase-Nicola, S., and and ten Wolde, P. R. (2006) Diffusion of transcription factors can drastically enhance the noise in gene expression Biophys. J. 91, 4350-4367 10.1529/biophysj.106.086157
61. de Jong, I. G., Haccou, P., and Kuipers, O. P. (2011) Bet hedging or not? A guide to proper classification of microbial survival strategies BioEssays 33, 215-223 10.1002/bies.201000127
62. Veening, J.-W., Smits, W. K., and Kuipers, O. P. (2008) Bistability, epigenetics, and bet-hedging in bacteria Annu. Rev. Microbiol. 62, 193-210 10.1146/annurev.micro.62.081307.163002
63. Delvigne, F. and Goffin, P. (2014) Microbial heterogeneity affects bioprocess robustness: Dynamic single-cell analysis contributes to understanding of microbial populations Biotechnol. J. 9, 61-72 10.1002/biot.201300119
64. Lou, C., Liu, X., Ni, M., Huang, Y., Huang, Q., Huang, L., Jiang, L., Lu, D., Wang, M., and Liu, C. (2010) Synthesizing a novel genetic sequential logic circuit: a push-on push-off switch Mol. Syst. Biol. 6, 350 10.1038/msb.2010.2
65. Abril, M. A., Michan, C., Timmis, K. N., and Ramos, J. L. (1989) Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway J. Bacteriol. 171, 6782-6790 10.1128/jb.171.12.6782-6790.1989
66. Martínez-García, E., Aparicio, T., Goñi-Moreno, A., Fraile, S., and de Lorenzo, V. (2015) SEVA 2.0: an update of the Standard European Vector Architecture for de-/re-construction of bacterial functionalities Nucleic Acids Res. 43, gku1114 10.1093/nar/gku1114
67. Keen, N. T., Tamaki, S., Kobayashi, D., and Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria Gene 70, 191-197 10.1016/0378-1119(88)90117-5
68. Schweizer, H. P. (2001) Vectors to express foreign genes and techniques to monitor gene expression in Pseudomonads Curr. Opin. Biotechnol. 12, 439-445 10.1016/S0958-1669(00)00242-1
69. Bao, Y., Lies, D. P., Fu, H., and Roberts, G. P. (1991) An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of gram-negative bacteria Gene 109, 167-168 10.1016/0378-1119(91)90604-A
70. Schmittgen, T. D. and Livak, K. J. (2008) Analyzing real-time PCR data by the comparative CT method Nat. Protoc. 3, 1101-1108 10.1038/nprot.2008.73
71. Gillespie, D. T. (1977) Exact stochastic simulation of coupled chemical reactions J. Phys. Chem. 81, 2340-2361 10.1021/j100540a008
72. Goñi-Moreno, A., Carcajona, M., Kim, J., Martinez-García, E., Amos, M., and de Lorenzo, V. (2016) An implementation-focused bio/algorithmic workflow for synthetic biology ACS Synth. Biol. 5, 1127 10.1021/acssynbio.6b00029
73. Goni-Moreno, A. and Amos, M. (2015) DiSCUS: A simulation platform for conjugation computing, In International Conference on Unconventional Computation and Natural Computation, pp 181-191, Springer.
74. Ho, J. W. K., Stefani, M., dos Remedios, C. G., and Charleston, M. A. (2008) Differential variability analysis of gene expression and its application to human diseases Bioinformatics 24, i390-i398 10.1093/bioinformatics/btn142
75. Vallet-Gely, I. and Boccard, F. (2013) Chromosomal organization and segregation in Pseudomonas aeruginosa PLoS Genet. 9, e1003492 10.1371/journal.pgen.1003492
76. Herrero, M., de Lorenzo, V., and Timmis, K. N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria J. Bacteriol. 172, 6557-6567 10.1128/jb.172.11.6557-6567.1990
77. Boyer, H. W. and Roulland-dussoix, D. (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli J. Mol. Biol. 41, 459-472 10.1016/0022-2836(69)90288-5
78. Nelson, K. E., Weinel, C., Paulsen, I. T., Dodson, R. J., Hilbert, H., Martins dos Santos, V. A. P., Fouts, D. E., Gill, S. R., Pop, M., and Holmes, M. (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440 Environ. Microbiol. 4, 799-808 10.1046/j.1462-2920.2002.00366.x
79. Bagdasarian, M., Lurz, R., Rückert, B., Franklin, F. C. H., Bagdasarian, M. M., Frey, J., and Timmis, K. N. (1981) Specific-purpose plasmid cloning vectors II. Broad host range, high copy number, RSF 1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas Gene 16, 237-247 10.1016/0378-1119(81)90080-9
80. Worsey, M. J. and Williams, P. A. (1975) Metabolism of toluene and xylenes by Pseudomonas (putida (arvilla) mt-2: evidence for a new function of the TOL plasmid J. Bacteriol. 124, 7-13
81. Kessler, B., Herrero, M., Timmis, K. N., and De Lorenzo, V. (1994) Genetic evidence that the XylS regulator of the Pseudomonas TOL meta operon controls the Pm promoter through weak DNA-protein interactions J. Bacteriol. 176, 3171-3176 10.1128/jb.176.11.3171-3176.1994
82. Choi, K.-H., Gaynor, J. B., White, K. G., Lopez, C., Bosio, C. M., Karkhoff-Schweizer, R. R., and Schweizer, H. P. (2005) A Tn7-based broad-range bacterial cloning and expression system Nat. Methods 2, 443-448 10.1038/nmeth765
83. Zobel, S., Benedetti, I., Eisenbach, L., de Lorenzo, V., Wierckx, N., and Blank, L. M. (2015) Tn7-Based device for calibrated heterologous gene expression in Pseudomonas putida ACS Synth. Biol. 4, 1341-1351 10.1021/acssynbio.5b00058