Transcriptional control of motility enables directional movement of Escherichia coli in a signal gradient

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Ravichandar, Jayamary Divya ^a   Bower, Adam G ^a,b   Julius, A Agung ^c   Collins, Cynthia H ^a,d  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c Rensselaer Polytechnic Institute   (United States)

^d Rensselaer Polytechnic Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC ENGINEERING; GENETICS; LOCOMOTION; MICROBIAL GENETICS; MOLECULAR BIOLOGY; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; THEORETICAL MODEL;

ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC ENGINEERING; GENETICS, MICROBIAL; LOCOMOTION; MODELS, THEORETICAL; MOLECULAR BIOLOGY; SIGNAL TRANSDUCTION;

EID: 85027893677     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-08870-6     Document Type: Article

References (56)

1. Sourjik, V., & Wingreen, N. S. Responding to chemical gradients: bacterial chemotaxis. Curr. Opin. Cell Biol. 24, 262-268 (2012
2. Guttenplan, S. B., & Kearns, D. B. Regulation of flagellar motility during biofilm formation. FEMS Microbiol. Rev. 37, 849-871 (2013
3. Kerr, B., Riley, M. A., Feldman, M. W., & Bohannan, B. J. M. Local dispersal promotes biodiversity in a real-life game of rock-paperscissors. Nature 418, 171-174 (2002
4. Salis, H., Tamsir, A., & Voigt, C. Bacterial Sensing and Signaling 16, 194-225 (KARGER, 2009
5. Tecon, R., & van der Meer, J. R. Bacterial biosensors for measuring availability of environmental pollutants. Sensors 8, 4062-4080 (2008
6. Voigt, C. A. Genetic parts to program bacteria. Curr. Opin. Biotechnol. 17, 548-557 (2006
7. Sinha, J., Reyes, S. J., & Gallivan, J. P. Reprogramming bacteria to seek and destroy an herbicide. Nat. Chem. Biol. 6, 464-470 (2010
8. Tien, S.-M., et al. Engineering bacteria to search for specific concentrations of molecules by a systematic synthetic biology design method. PLoS One 11, e0152146, doi: 10.1371/journal.pone.0152146. (2016
9. Weibel, D. B., et al. Microoxen: microorganisms to move microscale loads. Proc. Natl. Acad. Sci. USA 102, 11963-11967 (2005
10. Steager, E. B., Julius, A. A., Kim, M., Kumar, V., & Pappas, G. J. Modeling, control and experimental characterization of microbiorobots. Int. J. Rob. Res. 30, 647-658 (2011
11. Berg, H. C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72, 19-54 (2003
12. Li, H., & Sourjik, V. Assembly and stability of flagellar motor in Escherichia coli. Mol. Microbiol. 80, 886-899 (2011
13. Fahrner, K. A., Block, S. M., Krishnaswamy, S., Parkinson, J. S., & Berg, H. C. A mutant hook-associated protein (HAP3) facilitates torsionally induced transformations of the flagellar filament of Escherichia coli. J. Mol. Biol. 238, 173-186 (1994
14. Kojima, S., & Blair, D. F. Conformational Change in the Stator of the Bacterial Flagellar Motor. Biochemistry 40, 13041-13050 (2001
15. Sourjik, V., & Berg, H. C. Functional interactions between receptors in bacterial chemotaxis. Nature 428, 437-441 (2004
16. Parkinson, J. S. cheA, cheB and cheC genes of Escherichia coli and their role in chemotaxis. J. Bacteriol. 126, 758-770 (1976
17. Baker, M. D., Wolanin, P. M., & Stock, J. B. Signal transduction in bacterial chemotaxis. Bioessays 28, 9-22 (2006
18. Kuo, S. C., & Koshland, D. E. Roles of cheY and cheZ gene products in controlling flagellar rotation in bacterial chemotaxis of Escherichia coli. J. Bacteriol. 169, 1307-1314 (1987
19. Mishler, D. M., Topp, S., Reynoso, C. M. K., & Gallivan, J. P. Engineering bacteria to recognize and follow small molecules. Curr. Opin. Biotechnol. 21, 653-656 (2010
20. Liu, C., et al. Sequential establishment of stripe patterns in an expanding cell population. Science 334, 238-241 (2011
21. Weiss, L. E., et al. Engineering motility as a phenotypic response to LuxI/R-dependent quorum sensing in Escherichia coli. Biotechnol. Bioeng. 100, 1251-1255 (2008
22. Topp, S., & Gallivan, J. P. Guiding bacteria with small molecules and RNA. J. Am. Chem. Soc. 129, 6807-6811 (2007
23. Derr, P., Boder, E., & Goulian, M. Changing the specificity of a bacterial chemoreceptor. J. Mol. Biol. 355, 923-932 (2006
24. Bi, S., et al. Discovery of novel chemoeffectors and rational design of Escherichia coli chemoreceptor specificity. Proc. Natl. Acad. Sci. USA 110, 16814-16819 (2013
25. Bi, S., Pollard, A. M., Yang, Y., Jin, F., & Sourjik, V. Engineering hybrid chemotaxis receptors in bacteria. ACS Synth. Biol. 5, 989-1001 (2016
26. Ma, X., Hortelão, A. C., Patiño, T., & Sánchez, S. Enzyme catalysis to power micro/nanomachines. ACS Nano 10, 9111-9122 (2016
27. Muddana, H. S., Sengupta, S., Mallouk, T. E., Sen, A., & Butler, P. J. Substrate catalysis enhances single-enzyme diffusion. J. Am. Chem. Soc. 132, 2110-2111 (2010
28. Sengupta, S., et al. Enzyme molecules as nanomotors. J. Am. Chem. Soc. 135, 1406-1414 (2013
29. Dey, K. K., et Al. Micromotors Powered by Enzyme Catalysis. Nano Lett. 15, 8311-8315 (2015
30. Ng, W.-L., & Bassler, B. L. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43, 197-222 (2009
31. Papenfort, K., & Bassler, B. L. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14, 576-588 (2016
32. Choudhary, S., & Schmidt-Dannert, C. Applications of quorum sensing in biotechnology. Appl. Microbiol. Biotechnol. 86, 1267-1279 (2010
33. Garg, N., Manchanda, G., & Kumar, A. Bacterial quorum sensing: circuits and applications. Antonie Van Leeuwenhoek 105, 289-305 (2014
34. Basu, S., Gerchman, Y., Collins, C. H., Arnold, F. H., & Weiss, R. A synthetic multicellular system for programmed pattern formation. Nature 434, 1130-4 (2005
35. Anderson, J. C., Clarke, E. J., Arkin, A. P., & Voigt, C. A. Environmentally controlled invasion of cancer cells by engineered bacteria. J. Mol. Biol. 355, 619-27 (2006
36. Moon, T. S., Lou, C., Tamsir, A., Stanton, B. C., & Voigt, C. A. Genetic programs constructed from layered logic gates in single cells. Nature 491, 249-253 (2012
37. Hennig, S., et al. Artificial cell-cell communication as an emerging tool in synthetic biology applications. J. Biol. Eng. 9, 13 (2015
38. Wang, Z., et al. Artificially constructed quorum-sensing circuits are used for subtle control of bacterial population density. PLoS One 9, e104578, doi: 10.1371/journal.pone.0104578 (2014
39. Garza, A. G., Bronstein, P. A., Valdez, P. A., Harris-Haller, L. W., & Manson, M. D. Extragenic suppression of motA missense mutations of Escherichia coli. J. Bacteriol. 178, 6116-6122 (1996
40. Garza, A. G., Harris-Haller, L. W., Stoebner, R. A., & Manson, M. D. Motility protein interactions in the bacterial flagellar motor. Proc. Natl. Acad. Sci. USA 92, 1970-1974 (1995
41. Blair, D. F., & Berg, H. C. Restoration of torque in defective flagellar motors. Science 242, 1678-1681 (1988
42. Minogue, T. D., Wehland-von Trebra, M., Bernhard, F., & Von Bodman, S. B. The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol. Microbiol. 44, 1625-1635 (2002
43. Shong, J., Huang, Y.-M., Bystroff, C., & Collins, C. H. Directed evolution of the quorum-sensing regulator esar for increased signal sensitivity. ACS Chem. Biol. 8, 789-795 (2013
44. Seila, A. C., Core, L. J., Lis, J. T., & Sharp, P. A. Divergent transcription: a new feature of active promoters. Cell Cycle 8, 2557-2564 (2009
45. Toews, M. L., Goy, M. F., Springer, M. S., & Adler, J. Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. Proc. Natl. Acad. Sci. USA 76, 5544-5548 (1979
46. Bren, A., & Eisenbach, M. How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J. Bacteriol. 182, 6865-6873 (2000
47. Vogel, U., & Jensen, K. F. The RNA chain elongation rate in Escherichia coli depends on the growth rate. J. Bacteriol. 176, 2807-2813 (1994
48. Milo, R., Jorgensen, P., Moran, U., Weber, G., & Springer, M. BioNumbers-the database of key numbers in molecular and cell biology. Nucleic Acids Res. 38, D750-3 (2010
49. Steager, E. B., et al. Electrokinetic and optical control of bacterial microrobots. J. Micromechanics Microengineering 21, 035001 (2011
50. Karig, D., & Weiss, R. Signal-amplifying genetic circuit enables in vivo observation of weak promoter activation in the Rhl quorum sensing system. Biotechnol. Bioeng. 89, 709-718 (2005
51. Tamsir, A., Tabor, J. J., & Voigt, C. A. Robust multicellular computing using genetically encoded NOR gates and chemical ?wires?. Nature 469, 212-215 (2011
52. Shong, J., & Collins, C. H. Quorum sensing-modulated AND-gate promoters control gene expression in response to a combination of endogenous and exogenous signals. (2013
53. Salis, H. M., Mirsky, E. A., & Voigt, C. A. Automated design of synthetic ribosome binding sites to control protein expression. Nat. Biotechnol. 27, 946-950 (2009
54. Espah Borujeni, A., Channarasappa, A. S., & Salis, H. M. Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites. Nucleic Acids Res. 42, 2646-2659 (2014
55. Shong, J., & Collins, C. H. Engineering the esaR promoter for tunable quorum sensing-dependent gene expression. ACS Synth. Biol. 2, 568-75 (2013
56. Shong, J. Quorum-sensing repressor-based tools for cell-cell communication in synthetic biology. PhD thesis, Rensselaer Polytechnic Institute, Department of Chemical and Biological Engineering (2013