The evolution of the bacterial luciferase gene cassette (lux) as a real-time bioreporter

Sensors

Volumn 12, Issue 1, 2012, Pages 732-752

  Close, Dan ^a   Xu, Tingting ^a   Smartt, Abby ^b   Rogers, Alexandra ^b   Crossley, Robert ^b   Price, Sarah ^b   Ripp, Steven ^b   Sayler, Gary ^a,b  

^a OAK RIDGE NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Bacterial luciferase (lux); Bioreporter; Biosensor; Cell culture; Mammalian cells; Small animal models

Indexed keywords

LUCIFERASE;

BACTERIAL GENE; EUKARYOTIC CELL; GENETICS; LUMINESCENCE; METABOLISM; METHODOLOGY; REPORTER GENE; REVIEW; TIME;

EUKARYOTIC CELLS; GENES, BACTERIAL; GENES, REPORTER; LUCIFERASES; LUMINESCENT MEASUREMENTS; TIME FACTORS;

EID: 84856276040     PISSN: 14248220     EISSN: None     Source Type: Journal    
DOI: 10.3390/s120100732     Document Type: Review

References (84)

1. Close, D.M.; Ripp, S.; Sayler, G.S. Reporter proteins in whole-cell optical bioreporter detection systems, biosensor integrations, and biosensing applications. Sensors 2009, 9, 9147-9174.
2. McElroy, W.; Hastings, J.; Sonnenfeld, V.; Coulombre, J. The requirement of riboflavin phosphate for bacterial luminescence. Science 1953, 118, 385-386.
3. Strehler, B.; Harvey, E.; Chang, J.; Cormier, M. The luminescent oxidation of reduced riboflavin or reduced riboflavin phosphate in the bacterial luciferin-luciferase reaction. Proc. Natl. Acad. Sci. USA 1954, 40, 10-12.
4. Belas, R.; Mileham, A.; Cohn, D.; Hilmen, M.; Simon, M.; Silverman, M. Bacterial bioluminescence: Isolation and expression of the luciferase genes from Vibrio harveyi. Science 1982, 218, 791-793.
5. Gupta, R.K.; Patterson, S.S.; Ripp, S.; Sayler, G.S. Expression of the Photorhabdus luminescens lux genes (luxA, B, C, D, and E) in Saccharomyces cerevisiae. FEMS Yeast Res. 2003, 4, 305-313.
6. Patterson, S.S.; Dionisi, H.M.; Gupta, R.K.; Sayler, G.S. Codon optimization of bacterial luciferase (lux) for expression in mammalian cells. J. Ind. Microbiol. Biotechnol. 2005, 32, 115-123.
7. Close, D.M.; Patterson, S.S.; Ripp, S.; Baek, S.J.; Sanseverino, J.; Sayler, G.S. Autonomous bioluminescent expression of the bacterial luciferase gene cassette (lux) in a mammalian cell line. PLoS One 2010, 5, e12441.
8. Nealson, K.H.; Hastings, J. Bacterial bioluminescence: Its control and ecological significance. Microbiol. Mol. Biol. Rev. 1979, 43, 496-518.
9. Meighen, E.A. Molecular biology of bacterial bioluminescence. Microbiol. Rev. 1991, 55, 123-142.
10. Swartzman, E.; Silverman, M.; Meighen, E. The luxR gene product of Vibrio harveyi is a transcriptional activator of the lux promoter. J. Bacteriol. 1992, 174, 7490-7493.
11. Engebrecht, J.; Nealson, K.; Silverman, M. Bacterial bioluminescence: Isolation and genetic analysis of functions from Vibrio fischeri. Cell 1983, 32, 773-781.
12. Fernandezpinas, F.; Wolk, C. Expression of luxCD-E in Anabeaena sp. can replace the use of exogenous aldehyde for in vivo localization of transcription by luxAB. Gene 1994, 150, 169-174.
13. Frackman, S.; Anhalt, M.; Nealson, K. Cloning, organization, and expression of the bioluminescence genes of Xenorhabdus luminescens. J. Bacteriol. 1990, 172, 5767-5773.
14. Engebrecht, J.; Simon, M.; Silverman, M. Measuring gene expression with light. Science 1985, 227, 1345-1347.
15. Belas, R.; Simon, M.; Silverman, M. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J. Bacteriol. 1986, 167, 210-218.
16. Shaw, J.J.; Kado, C.I. Development of a Vibrio bioluminescence gene set to monitor phytopathogenic bacteria during the ongoing disease process in a nondisruptive manner. Nat. Biotechnol. 1986, 4, 560-564.
17. de Weger, L.; Dunbar, P.; Mahafee, F.; Lugtenberg, B.; Sayler, G. Use of bioluminescence markers to detect Pseudomonas spp. in the rhizosphere. Appl. Environ. Microbiol. 1991, 57, 3641-3644.
18. Ripp, S.; Nivens, D.E.; Ahn, Y.; Werner, C.; Jarrell, J.; Easter, J.P.; Cox, C.D.; Burlage, R.S.; Sayler, G.S. Controlled field release of a bioluminescent genetically engineered microorganism for bioremediation process monitoring and control. Environ. Sci. Technol. 2000, 34, 846-853.
19. King, J.M.H.; Digrazia, P.M.; Applegate, B.; Burlage, R.; Sanseverino, J.; Dunbar, P.; Larimer, F.; Sayler, G.S. Rapid, sensitive bioluminescent reporter technology for naphthalene exposure and biodegradation. Science 1990, 249, 778-781.
20. Burlage, R.S.; Sayler, G.S.; Larimer, F. Monitoring of naphthalene catabolism by bioluminescence with nah-lux transcriptional fusions. J. Bacteriol. 1990, 172, 4749-4757.
21. Applegate, B.M.; Kehrmeyer, S.R.; Sayler, G.S. A chromosomally based tod-luxCDABE whole-cell reporter for benzene, toluene, ethybenzene, and xylene (BTEX) sensing. Appl. Environ. Microbiol. 1998, 64, 2730-2735.
22. Abd-El-Haleem, D.; Ripp, S.; Scott, C.; Sayler, G.S. A luxCDABE-based bioluminescent bioreporter for the detection of phenol. J. Ind. Microbiol. Biotechnol. 2002, 29, 233-237.
23. Davidov, Y.; Rozen, R.; Smulski, D.R.; Van Dyk, T.K.; Vollmer, A.C.; Elsemore, D.A.; LaRossa, R.A.; Belkin, S. Improved bacterial SOS promoter::lux fusions for genotoxicity detection. Mutat. Res. 2000, 466, 97-107.
24. Belkin, S.; Gu, M. Whole Cell Sensing Systems II: Applications; Springer-Verlag: Berlin, Germany, 2010.
25. Ripp, S.; Layton, A.C.; Sayler, G.S. The microbe as a reporter: Microbial bioreporter sensing technologies for chemical and biological detection. In Environmental Microbiology: Current Technology and Water Applications; Sen, K., Ashbolt, N.J., Eds.; Caister Academic Press: Norfolk, UK, 2011; pp. 281-305.
26. Hay, A.G.; Rice, J.F.; Applegate, B.M.; Bright, N.G.; Sayler, G.S. A bioluminescent whole-cell reporter for detection of 2,4-dichlorophenoxyacetic acid and 2,4-dichlorophenol in soil. Appl. Environ. Microbiol. 2000, 66, 4589-4594.
27. Toba, F.A.; Hay, A.G. A simple solid phase assay for the detection of 2,4-D in soil. J. Microbiol. Methods 2005, 62, 135-143.
28. Burlage, R.S. Organic contaminant detection and biodegradation characteristics. In Methods in Molecular Biology/Bioluminescence; LaRossa, R., Ed.; Humana Press: Totowa, NJ, USA, 1998; pp. 259-268.
29. Rozen, Y.; Nejidat, A.; Gartemann, K.H.; Belkin, S. Specific detection of p-chlorobenzoic acid by Escherichia coli bearing a plasmid-borne fcbA'::lux fusion. Chemosphere 1999, 38, 633-641.
30. Wallace, W.H.; Fleming, J.T.; White, D.C.; Sayler, G.S. An algD-lux bioluminescent reporter plasmid to monitor alginate production in biofilms. Microb. Ecol. 1994, 27, 225-239.
31. Simpson, M.L.; Paulus, M.J.; Jellison, G.E.; Sayler, G.S.; Nivens, D.E.; Dionisi, H.M.; Ripp, S.; Applegate, B.; Patterson, G.; Bolton, E.; et al. Bioluminescent bioreporter integrated circuits (BBICs): Whole-cell environmental monitoring devices. In Proceedings of the 30th International Conference on Environmental Systems (Society of Automotive Engineers), Toulouse, France, 10-13 July 2000.
32. Eldridge, M.L.; Sanseverino, J.; Layton, A.C.; Easter, J.P.; Schultz, T.W.; Sayler, G.S. Saccharomyces cerevisiae BLYAS, a new bioluminescent bioreporter for detection of androgenic compounds. Appl. Environ. Microbiol. 2007, 73, 6012-6018.
33. Francis, K.P.; Joh, D.; Bellinger-Kawahara, C.; Hawkinson, M.J.; Purchio, T.F.; Contag, P.R. Monitoring bioluminescent Staphylococcus aureus infections in mice using a novel luxABCDE construct. Infect. Immun. 2000, 68, 3594-3600.
34. Flynn, H.C.; Meharg, A.A.; Bowyer, P.K.; Paton, G.I. Antimony bioavailability in mine soils. Environ. Pollut. 2003, 124, 93-100.
35. Ivask, A.; Green, T.; Polyak, B.; Mor, A.; Kahru, A.; Virta, M.; Marks, R. Fibre-optic bacterial biosensors and their application for the analysis of bioavailable Hg and As in soils and sediments from Aznalcollar mining area in Spain. Biosens. Bioelectron. 2007, 22, 1396-1402.
36. Corbisier, P.; Thiry, E.; Diels, L. Bacterial biosensors for the toxicity assessment of solid waste. Environ. Toxicol. Water Qual. 1996, 11, 171-177.
37. Peitzsch, N.; Eberz, G.; Nies, D.H. Alcaligenes eutrophus as a bacterial chromate sensor. Appl. Environ. Microbiol. 1998, 64, 453-458.
38. Tibazarwa, C.; Wuertz, S.; Mergeay, M.; Wyns, L.; van der Lelie, D. Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J. Bacteriol. 2000, 182, 1399-1409.
39. Riether, K.B.; Dollard, M.A.; Billard, P. Assessment of heavy metal bioavailability using Escherichia coli zntAp::lux and copAp::lux based biosensors. Appl. Microbiol. Biotechnol. 2001, 57, 712-716.
40. Lopes, N.; Hawkins, S.; Jegier, P.; Menn, F.-M.; Sayler, G.; Ripp, S. Detection of dichloromethane with a bioluminescent (lux) bacterial bioreporter. J. Ind. Microbiol. Biotechnol. 2012, 39, 45-53.
41. Belkin, S.; Smulski, D.R.; Dadon, S.; Vollmer, A.C.; Van Dyk, T.K.; LaRossa, R.A. A panel of stress-responsive luminous bacteria for the detection of selected classes of toxicants. Wat. Res. 1997, 31, 3009-3016.
42. Vollmer, A.C.; Belkin, S.; Smulski, D.R.; Van Dyk, T.K.; LaRossa, R.A. Detection of DNA damage by use of Escherichia coli carrying recA'-lux, uvrA'-lux, or alkA'-lux reporter plasmids. Appl. Environ. Microbiol. 1997, 63, 2566-2571.
43. Hwang, E.T.; Ahn, J.M.; Kim, B.C.; Gu, M.B. Construction of a nrdA::luxCDABE fusion and its use in Escherichia coli as a DNA damage biosensor. Sensors 2008, 8, 1297-1307.
44. van Dyk, T.K.; DeRose, E.J.; Gonye, G.E. LuxArray, a high-density, genomewide transcription analysis of Escherichia coli using bioluminescent reporter strains. J. Bacteriol. 2001, 183, 5496-5505.
45. Sanseverino, J.; Gupta, R.K.; Layton, A.C.; Patterson, S.S.; Ripp, S.A.; Saidak, L.; Simpson, M.L.; Schultz, T.W.; Sayler, G.S. Use of Saccharomyces cerevisiae BLYES expressing bacterial bioluminescence for rapid, sensitive detection of estrogenic compounds. Appl. Environ. Microbiol. 2005, 71, 4455-4460.
46. Min, J.; Lee, C.W.; Moon, S.H.; LaRossa, R.A.; Gu, M.B. Detection of radiation effects using recombinant bioluminescent Escherichia coli strains. Radiat. Environ. Biophys. 2000, 39, 41-45.
47. Rupani, S.P.; Gu, M.B.; Konstantinov, K.B.; Dhurjati, P.S.; Van Dyk, T.K.; Larossa, R.A. Characterization of the stress response of a bioluminescent biological sensor in batch and continuous cultures. Biotechnol. Prog. 1996, 12, 387-392.
48. van Dyk, T.K.; Reed, T.R.; Vollmer, A.C.; LaRossa, R.A. Synergistic induction of the heat shock response in Escherichia coli by simultaneous treatment with chemical inducers. J. Bacteriol. 1995, 177, 6001-6004.
49. Jouanneau, S.; Durand, M.J.; Courcoux, P.; Blusseau, T.; Thouand, G. Improvement of the identification of four heavy metals in environmental samples by using predictive decision tree models coupled with a set of five bioluminescent bacteria. Environ. Sci. Technol. 2011, 45, 2925-2931.
50. Bang, Y.B.; Lee, S.E.; Rhee, J.H.; Choi, S.H. Evidence that expression of the Vibrio vulnificus hemolysin gene is dependent on cyclic AMP and cyclic AMP receptor protein. J. Bacteriol. 1999, 181, 7639-7642.
51. Belkin, S.; Smulski, D.R.; Vollmer, A.C.; Van Dyk, T.K.; LaRossa, R.A. Oxidative stress detection with Escherichia coli harboring a katG'::lux fusion. Appl. Environ. Microbiol. 1996, 62, 2252-2256.
52. Contag, C.H.; Contag, P.R.; Mullins, J.I.; Spilman, S.D.; Stevenson, D.K.; Benaron, D.A. Photonic detection of bacterial pathogens in living hosts. Mol. Microbiol. 1995, 18, 593-603.
53. Khang, Y.H.; Yang, Z.K.; Burlage, R.S. Measurement of iron-dependence of pupA promoter activity by a pup-lux bioreporter. J. Microbiol. Biotechnol. 1997, 7, 352-355.
54. Selifonova, O.V.; Eaton, R.W. Use of an ipb-lux fusion to study regulation of the isopropylbenzene catabolism operon of Pseudomonas putida RE204 and to detect hydrophobic pollutants in the environment. Appl. Environ. Microbiol. 1996, 62, 778-783.
55. Magrisso, S.; Belkin, S.; Erel, Y. Lead bioavailability in soil and soil components. Water Air Soil Pollut. 2009, 202, 315-323.
56. Larose, C.; Dommergue, A.; Marusczak, N.; Coves, J.; Ferrari, C.P.; Schneider, D. Bioavailable mercury cycling in polar snowpacks. Environ. Sci. Technol. 2011, 45, 2150-2156.
57. Yan, L.; Allen, M.S.; Simpson, M.L.; Sayler, G.S.; Cox, C.D. Direct quantification of N-(3-oxo-hexanoyl)-L-homoserine lactone in culture supernatant using a whole-cell bioreporter. J. Microbiol. Methods 2007, 68, 40-45.
58. Heitzer, A.; Webb, O.F.; Thonnard, J.E.; Sayler, G.S. Specific and quantitative assessment of naphthalene and salicylate bioavailability by using a bioluminescent catabolic reporter bacterium. Appl. Environ. Microbiol. 1992, 58, 1839-1846.
59. Everhart, J.L.; McNear, D.; Peltier, E.; van der Lelie, D.; Chaney, R.L.; Sparks, D.L. Assessing nickel bioavailability in smelter-contaminated soils. Sci. Total Environ. 2006, 367, 732-744.
60. Abd-El-Haleem, D.; Ripp, S.; Zaki, S.; Sayler, G.S. Detection of nitrate/nitrite bioavailability in wastewater using a luxCDABE-based Klebsiella oxytoca bioluminescent bioreporter. J. Microbiol. Biotechnol. 2007, 17, 1254-1261.
61. Lee, H.J.; Gu, M.B. Construction of a sodA::luxCDABE fusion Escherichia coli: Comparison with a katG fusion strain through their responses to oxidative stresses. Appl. Microbiol. Biotechnol. 2003, 60, 577-580.
62. Layton, A.C.; Muccini, M.; Ghosh, M.M.; Sayler, G.S. Construction of a bioluminescent reporter strain to detect polychlorinated biphenyls. Appl. Environ. Microbiol. 1998, 64, 5023-5026.
63. Ripp, S.; Applegate, B.; Nivens, D.E.; Simpson, M.L.; Sayler, G.S. Advances in whole-cell bioluminescent bioreporters for environmental monitoring and chemical sensing. In Proceedings of the AIChE Annual Meeting, Los Angeles, CA, USA, 12-17 November 2000.
64. Shimizu, T.; Ohta, Y.; Tsutsuki, H.; Noda, M. Construction of a novel bioluminescent reporter system for investigating Shiga toxin expression of enterohemorrhagic Escherichia coli. Gene 2011, 478, 1-10.
65. Hansen, L.H.; Sorensen, S.J. Detection and quantification of tetracyclines by whole cell biosensors. FEMS Microbiol. Lett. 2000, 190, 273-278.
66. Elad, T.; Benovich, E.; Magrisso, S.; Belkin, S. Toxicant identification by a luminescent bacterial bioreporter panel: Application of pattern classification algorithms. Environ. Sci. Technol. 2008, 42, 8486-8491.
67. Elad, T.; Lee, J.H.; Gu, M.B.; Belkin, S. Microbial cell arrays. In Whole Cell Sensing Systems I: Reporter Cells and Devices; Belkin, S., Gu, M.B., Eds.; Springer: Berlin, Germany, 2010; Volume 117, pp. 85-108.
68. Shingleton, J.T.; Applegate, B.M.; Nagel, A.C.; Bienkowski, P.R.; Sayler, G.S. Induction of the tod operon by trichloroethylene in Pseudomonas putida TVA8. Appl. Environ. Microbiol. 1998, 64, 5049-5052.
69. Burlage, R.S.; Patek, D.R.; Everman, K.R. Method for Detection of Buried Explosives Using a Biosensor. U.S. Patent 5,972,638, October 1999.
70. Vollmer, A.C.; Kwakye, S.; Halpern, M.; Everbach, E.C. Bacterial stress response to 1-megahertz pulsed ultrasound in the presence of microbubbles. Appl. Environ. Microbiol. 1998, 64, 3927-3931.
71. Elasri, M.O.; Miller, R.V. A Pseudomonas aeruginosa biosensor responds to exposure to ultraviolet radiation. Appl. Microbiol. Biotechnol. 1998, 50, 455-458.
72. Bakhrat, A.; Eltzov, E.; Finkelstein, Y.; Marks, R.S.; Raveh, D. UV and arsenate toxicity: A specific and sensitive yeast bioluminescence assay. Cell Biol. Toxicol. 2011, 27, 227-236.
73. Erbe, J.L.; Adams, A.C.; Taylor, K.B.; Hall, L.M. Cyanobacteria carrying an smt-lux transcriptional fusion as biosensors for the detection of heavy metal cations. J. Ind. Microbiol. 1996, 17, 80-83.
74. Almashanu, S.; Musafia, B.; Hadar, R.; Suissa, M.; Kuhn, J. Fusion of luxA and luxB and its expression in Escherichia coli, Saccharomyces cerevisiae and Drosophila melanogaster. J. Biolumin. Chemilumin. 1990, 5, 89-97.
75. Kirchner, G.; Roberts, J.L.; Gustafson, G.D.; Ingolia, T.D. Active bacterial luciferase from a fused gene: Expression of a Vibrio harveyi luxAB translational fusion in bacteria, yeast and plant cells. Gene 1989, 81, 349-354.
76. Olsson, O.; Koncz, C.; Szalay, A.A. The use of the luxA gene of the bacterial luciferase operon as a reporter gene. Mol. Gen. Genet. 1988, 215, 1-9.
77. Close, D.; Hahn, R.; Ripp, S.; Sayler, G.S. Determining toxicant bioavailability using a constitutively bioluminescent human cell line. In Proceedings for the 3rd Annual Biomedical Science and Engineering Conference, Oak Rige, TN, USA, 15-17 March 2011.
78. Close, D.M.; Hahn, R.; Patterson, S.S.; Ripp, S.; Sayler, G.S. Comparison of human optimized bacterial luciferase, firefly luciferase, and green fluorescent protein for continuous imaging of cell culture and animal models. J. Biomed. Opt. 2011, 16, e12441.
79. Craney, A.; Hohenauer, T.; Xu, Y.; Navani, N.K.; Li, Y.F.; Nodwell, J. A synthetic luxCDABE gene cluster optimized for expression in high-GC bacteria. Nucleic Acids Res. 2007, doi: 10.1093/nar/gkm086.
80. Yagur-Kroll, S.; Belkin, S. Upgrading bioluminescent bacterial bioreporter performance by splitting the lux operon. Anal. Bioanal. Chem. 2011, 400, 1071-1082.
81. Nivens, D.E.; McKnight, T.E.; Moser, S.A.; Osbourn, S.J.; Simpson, M.L.; Sayler, G.S. Bioluminescent bioreporter integrated circuits: Potentially small, rugged and inexpensive whole-cell biosensors for remote environmental monitoring. J. Appl. Microbiol. 2004, 96, 33-46.
82. Ripp, S.; DiClaudio, M.; Sayler, G. Biosensors as environmental monitors. In Environmental Microbiology, 2nd ed.; Mitchell, R., Gu, J., Eds.; Wiley-Blackwell: Hoboken, NJ, USA, 2010; pp. 213-233.
83. Vijayaraghavan, R.; Islam, S.; Zhang, M.; Ripp, S.; Caylor, S.; Bull, N.D.; Moser, S.; Terry, S.; Blalock, B.; Sayler, G. A bioreporter bioluminescent integrated circuit for very low-level chemical sensing in both gas and liquid environments. Sens. Actuat. B-Chem. 2007, 123, 922-928.
84. Simpson, M.L.; Sayler, G.S.; Applegate, B.M.; Ripp, S.; Nivens, D.E.; Paulus, M.J.; Jellison, G.E. Bioluminescent-bioreporter integrated circuits form novel whole-cell biosensors. Trends Biotechnol. 1998, 16, 332-338.