Can the natural diversity of quorum-sensing advance synthetic biology?

Frontiers in Bioengineering and Biotechnology

Volumn 3, Issue MAR, 2015, Pages

  Davis, René Michele ^a   Muller, Ryan Yue ^a,b   Haynes, Karmella Ann ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Crosstalk; Genetic wire; Homoserine lactone; Orthogonal; Quorum sensing; Synthetic gene circuit

Indexed keywords

EID: 85042577902     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2015.00030     Document Type: Review

References (67)

1. Anderson, J. C., Clarke, E. J., Arkin, A. P., and Voigt, C. A. (2006). Environmentally controlled invasion of cancer cells by engineered bacteria. J. Mol. Biol. 355, 619-627. doi:10.1016/j.jmb.2005.10.076.
2. Anesiadis, N., Kobayashi, H., Cluett, W. R., and Mahadevan, R. (2013). Analysis and design of a genetic circuit for dynamic metabolic engineering. ACS Synth. Biol. 2, 442-452. doi:10.1021/sb300129j.
3. Balagaddé, F. K., Song, H., Ozaki, J., Collins, C. H., Barnet, M., Arnold, F. H., et al. (2008). A synthetic Escherichia coli predator-prey ecosystem. Mol. Syst. Biol. 4, 187. doi:10.1038/msb.2008.24.
4. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., et al. (2000). The protein data bank www.rcsb.org. Nucleic Acids Res. 28, 235-242. doi:10.1093/nar/28.1.235.
5. Bernstein, H., Paulson, S., and Carlson, R. (2012). Synthetic Escherichia coli consortia engineered for syntrophy demonstrate enhanced biomass productivity. J. Biotechnol. 157, 159-166. doi:10.1016/j.jbiotec.2011.10.001.
6. Bottomley, M. J., Muraglia, E., Bazzo, R., and Carfí, A. (2007). Molecular insights into quorum sensing in the human pathogen Pseudomonas aeruginosa from the structure of the virulence regulator LasR bound to its autoinducer. J. Biol. Chem. 282, 13592-13600. doi:10.1074/jbc. M700556200.
7. Brenner, K., Karig, D. K., Weiss, R., and Arnold, F. H. (2007). Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proc. Natl. Acad. Sci. U.S.A. 104, 17300-17304. doi:10.1073/pnas.0704256104.
8. Canton, B., Labno, A., and Endy, D. (2008). Refinement and standardization of synthetic biological parts and devices. Nat. Biotechnol. 26, 787-793. doi:10.1038/nbt1413.
9. Case, R. J., Labbate, M., and Kjelleberg, S. (2008). AHL-driven quorum-sensing circuits: their frequency and function among the proteobacteria. ISME J. 2, 345-349. doi:10.1038/ismej.2008.13.
10. Chen, G., Swem, L. R., Swem, D. L., Stauff, D. L., O'Loughlin, C. T., Jeffrey, P. D., et al. (2011). A strategy for antagonizing quorum sensing. Mol. Cell 42, 199-209. doi:10.1016/j.molcel.2011.04.003.
11. Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., Bassler, B., et al. (2002). Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415, 545-549. doi:10.1038/415545a.
12. Cole, C., Barber, J., and Barton, G. (2008). The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 1, W197-W201. doi:10.1093/nar/gkn238.
13. Collins, C. H., Leadbetter, J. R., and Arnold, F. H. (2006). Dual selection enhances the signaling specificity of a variant of the quorum-sensing transcriptional activator LuxR. Nat. Biotechnol. 24, 708-712. doi:10.1038/nbt0806-1033c.
14. Connell, J. L., Ritschdorff, E. T., Whiteley, M., and Shear, J. B. (2013). 3D printing of microscopic bacterial communities. Proc. Natl. Acad. Sci. U.S.A. 110, 18380-18385. doi:10.1073/pnas.1309729110.
15. Daniel, R., Rubens, J. R., Sarpeshkar, R., and Lu, T. K. (2013). Synthetic analog computation in living cells. Nature 497, 619-623. doi:10.1038/nature12148.
16. Danino, T., Mondragón-Palomino, O., Tsimring, L., and Hasty, J. (2010). A synchronized quorum of genetic clocks. Nature 463, 326-330. doi:10.1038/nature08753.
17. Dickschat, J. S. (2010). Quorum sensing and bacterial biofilms. Nat. Prod. Rep. 27, 343-369. doi:10.1039/b804469b.
18. Eberl, L. (1999). N-acyl homoserinelactone-mediated gene regulation in gram-negative bacteria. Syst. Appl. Microbiol. 22, 493-506. doi:10.1016/S0723-2020(99)80001-0.
19. Egland, K., and Greenberg, E. (2001). Quorum sensing in Vibrio fischeri-analysis of the LuxR DNA binding region by alanine-scanning mutagenesis. J. Bacteriol. 183, 382-386. doi:10.1128/JB.183.1.382-386.2001.
20. Engebrecht, J., and Silverman, M. (1984). Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. U.S.A. 81, 4154-4158. doi:10.1073/pnas.81.13.4154.
21. Fink, J., and Hamilton, N. (2007). Domaindraw: a macromolecular feature drawing program. In silico Biol. 7, 145-150.
22. Fuqua, C., Winans, S. C., and Greenberg, E. P. (1996). Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu. Rev. Microbiol. 50, 727-751. doi:10.1146/annurev.micro.50.1.727.
23. Geske, G., Mattmann, M., and Blackwell, H. (2008). Evaluation of a focused library of N-aryl l-homoserine lactones reveals a new set of potent quorum sensing modulators. Bioorg. Med. Chem. Lett. 18, 5978-5981. doi:10.1016/j.bmcl.2008.07.089.
24. Goñi-Moreno, A., Amos, M., and de la Cruz, F. (2013). Multicellular computing using conjugation for wiring. PLoS ONE 8:e65986. doi:10.1371/journal.pone.0065986.
25. Gupta, S., Bram, E. E., and Weiss, R. (2013). Genetically programmable pathogen sense and destroy. ACS Synth. Biol. 2, 715-723. doi:10.1021/sb4000417.
26. Ji, W., Shi, H., Zhang, H., Sun, R., Xi, J., Wen, D., et al. (2013). A formalized design process for bacterial consortia that perform logic computing. PLoS ONE 8:e57482. doi:10.1371/journal.pone.0057482.
27. Kaplan, H., and Greenberg, E. P. (1987). Overproduction and purification of the luxR gene product: transcriptional activator of the Vibrio fischeri luminescence system. Proc. Natl. Acad. Sci. U.S.A. 84, 6639-6643. doi:10.1073/pnas.84.19.6639.
28. Kleerebezem, M., Quadri, L. E. N., Kuipers, O., and de Vos, W. (1997). Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol. Microbiol. 24, 895-904. doi:10.1046/j.1365-2958.1997.4251782.x.
29. Koseska, A., Zaikin, A., Kurths, J., and García-Ojalvo, J. (2009). Timing cellular decision making under noise via cell-cell communication. PLoS ONE 4:e4872. doi:10.1371/journal.pone.0004872.
30. Kumari, A., Pasini, P., Deo, S. K., Flomenhoft, D., Shashidhar, H., and Daunert, S. (2006). Biosensing systems for the detection of bacterial quorum signaling molecules. Anal. Chem. 78, 7603-7609. doi:10.1021/ac061421n.
31. Leung, M., Brimacombe, C., Spiegelman, G., and Beatty, J. (2012). The GtaR protein negatively regulates transcription of the gtaRI operon and modulates gene transfer agent (RcGTA) expression in Rhodobacter capsulatus. Mol. Microbiol. 83, 759-774. doi:10.1111/j.1365-2958.2011.07963.x.
32. Lewenza, S., Visser, M. B., and Sokol, P. A. (2002). Interspecies communication between Burkholderia cepacia and Pseudomonas aeruginosa. Can. J. Microbiol. 48, 707-716. doi:10.1139/w02-079.
33. Lindemann, A., Pessi, G., Schaefer, A., Mattmann, M., Christensen, Q., Kessler, A., et al. (2011). Isovaleryl-homoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. U.S.A. 108, 16765-16770. doi:10.1073/pnas.1114125108.
34. Liu, C., Fu, X., Liu, L., Ren, X., Chau, C. K. L., Li, S., et al. (2011). Sequential establishment of stripe patterns in an expanding cell population. Science 334, 238-241. doi:10.1126/science.1209042.
35. Llamas, I., Keshavan, N., and González, J. (2004). Use of Sinorhizobium meliloti as an indicator for specific detection of long-chain N-acyl homoserine lactones. Appl. Environ. Microbiol. 70, 3715-3723. doi:10.1128/AEM.70.6.3715-3723.2004.
36. Marchand, N., and Collins, C. H. (2013). Peptide-based communication system enables Escherichia coli to Bacillus megaterium interspecies signaling. Biotechnol. Bioeng. 110, 3003-3012. doi:10.1002/bit.24975.
37. McMillen, D., Kopell, N., Hasty, J., and Collins, J. J. (2002). Synchronizing genetic relaxation oscillators by intercell signaling. Proc. Natl. Acad. Sci. U.S.A. 99, 679-684. doi:10.1073/pnas.022642299.
38. Michael, B., Smith, J., Swift, S., Heffron, F., and Ahmer, B. (2001). SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J. Bacteriol. 183, 5733-5742. doi:10.1128/JB.183.19.5733-5742.2001.
39. Miller, M. B., and Bassler, B. L. (2001). Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165-199. doi:10.1146/annurev.micro.55.1.165.
40. Mitchell, A., Chang, H., Daugherty, L., Fraser, M., Hunter, S., Lopez, R., et al. (2015). The Interpro protein families database: the classification resource after 15 years. Nucleic Acids Res. 43, D213-D221. doi:10.1093/nar/gku1241.
41. Moon, T., Lou, C., Tamsir, A., Stanton, B., and Voigt, C. (2012). Genetic programs constructed from layered logic gates in single cells. Nature 491, 249-253. doi:10.1038/nature11516.
42. Nasuno, E., Kimura, N., Fujita, M. J., Nakatsu, C. H., Kamagata, Y., and Hanada, S. (2012). Phylogenetically novel LuxI/LuxR-type quorum sensing systems isolated using a metagenomic approach. Appl. Environ. Microbiol. 78, 8067-8074. doi:10.1128/AEM.01442-12.
43. Pai, A., Srimani, J. K., Tanouchi, Y., and You, L. (2014). Generic metric to quantify quorum sensing activation dynamics. ACS Synth. Biol. 3, 220-227. doi:10.1021/sb400069w.
44. Pai, A., and You, L. (2009). Optimal tuning of bacterial sensing potential. Mol. Syst. Biol. 5, 286. doi:10.1038/msb.2009.43.
45. Payne, S., and You, L. (2014). Engineered cell-cell communication and its applications. Adv. Biochem. Eng. Biotechnol. 146, 97-121. doi:10.1007/10_2013_249.
46. Põllumaa, L., Alamäe, T., and Mäe, A. (2012). Quorum sensing and expression of virulence in pectobacteria. Sensors 12, 3327-3349. doi:10.3390/s120303327.
47. Prindle, A., Samayoa, P., Razinkov, I., Danino, T., Tsimring, L. S., and Hasty, J. (2012a). A sensing array of radically coupled genetic "biopixels.". Nature 481, 39-44. doi:10.1038/nature10722.
48. Prindle, A., Selimkhanov, J., Danino, T., Samayoa, P., Goldberg, A., Bhatia, S., et al. (2012b). Genetic circuits in Salmonella typhimurium. ACS Synth. Biol. 1, 458-464. doi:10.1021/sb300060e.
49. Reading, N. C., and Sperandio, V. (2006). Quorum sensing: the many languages of bacteria. FEMS Microbiol. Lett. 254, 1-11. doi:10.1111/j.1574-6968.2005.00001.x.
50. Ruby, E. G., and Nealson, K. H. (1976). Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica: a model of symbiosis based on bacterial studies. Biol. Bull. 151, 574-586. doi:10.2307/1540507.
51. Saeidi, N., Wong, C. K., Lo, T.-M., Nguyen, H. X., Ling, H., Leong, S. S. J., et al. (2011). Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Mol. Syst. Biol. 7, 1-11. doi:10.1038/msb.2011.55.
52. Shong, J., Huang, Y.-M., Bystroff, C., and Collins, C. H. (2013). Directed evolution of the quorum-sensing regulator EsaR for increased signal sensitivity. ACS Chem. Biol. 8, 789-795. doi:10.1021/cb3006402.
53. Sigrist, C., de Castro, E., Cerutti, L., Cuche, B., Hulo, N., Bridge, A., et al. (2013). New and continuing developments at PROSITE. Nucleic Acids Res. 41, D344-D347. doi:10.1093/nar/gks1067.
54. Tabor, J. J., Salis, H. M., Simpson, Z. B., Chevalier, A., Levskaya, A., Marcotte, E. M., et al. (2009). A synthetic genetic edge detection program. Cell 137, 1272-1281. doi:10.1016/j.cell.2009.04.048.
55. Tamsir, A., Tabor, J., and Voigt, C. (2011). Robust multicellular computing using genetically encoded NOR gates and chemical "wires.". Nature 469, 212-215. doi:10.1038/nature09565.
56. UniProt Consortium. (2014). Activities at the universal protein resource (UniProt). Nucleic Acids Res. 42, D191-D198. doi:10.1093/nar/gkt1140.
57. Vannini, A., Volpari, C., Gargioli, C., Muraglia, E., Cortese, R., de Francesco, R., et al. (2002). The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J. 21, 4393-4401. doi:10.1093/emboj/cdf459.
58. Vendeville, A., Winzer, K., Heurlier, K., Tang, C. M., and Hardie, K. R. (2005). Making "sense" of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3, 383-396. doi:10.1038/nrmicro1146.
59. Vinuselvi, P., and Lee, S. K. (2012). Engineered Escherichia coli capable of co-utilization of cellobiose and xylose. Enzyme Microb. Technol. 50, 1-4. doi:10.1016/j.enzmictec.2011.10.001.
60. von Bodman, S., Ball, J., Faini, M., Herrera, C., Minogue, T., Urbanowski, M., et al. (2003). The quorum sensing negative regulators EsaR and ExpREcc, homologues within the LuxR family, retain the ability to function as activators of transcription. J. Bacteriol. 185, 7001-7007. doi:10.1128/JB.185.23.7001-7007.2003.
61. Wang, B., Barahona, M., and Buck, M. (2013). A modular cell-based biosensor using engineered genetic logic circuits to detect and integrate multiple environmental signals. Biosens. Bioelectron. 40, 368-376. doi:10.1016/j.bios.2012.08.011.
62. Weber, M., and Buceta, J. (2013). Dynamics of the quorum sensing switch: stochastic and non-stationary effects. BMC Syst. Biol. 7:6. doi:10.1186/1752-0509-7-6.
63. Williams, P., Winzer, K., Chan, W. C., and Cámara, M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1119-1134. doi:10.1098/rstb.2007.2039.
64. Wu, F., Menn, D. J., and Wang, X. (2014). Article circuits: from unimodality to trimodality. Chem. Biol. 21, 1629-1638. doi:10.1016/j.chembiol.2014.10.008.
65. Yao, Y., Martinez-Yamout, M., Dickerson, T. J., Brogan, A. P., Wright, P. E., and Dyson, H. J. (2006). Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. J. Mol. Biol. 355, 262-273. doi:10.1016/j.jmb.2005.10.041.
66. You, L., Cox, R., Weiss, R., and Arnold, F. (2004). Programmed population control by cell-cell communication and regulated killing. Nature 428, 868-871. doi:10.1038/nature02491.
67. Zhang, R., Pappas, K. M., Brace, J. L., Miller, P. C., Oulmassov, T., Molyneaux, J. M., et al. (2002). Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417, 971-974. doi:10.1038/nature00833.