Abstract
Genetically engineered bacterial whole-cell biosensors are powerful tools that take advantage of bacterial proteins and pathways to allow for detection of a specific analyte. These biosensors have been employed for a broad range of applications, including the detection of bacterial quorum-sensing molecules (QSMs). Bacterial QSMs are the small molecules bacteria use for population density-dependent communication, a process referred to as quorum sensing (QS). Various research groups have investigated the presence of QSMs, including N-acyl homoserine lactones (AHLs) and autoinducer-2 (AI-2), in physiological samples in attempts to enhance our knowledge of the role of bacteria and QS in disease states. Continued studies in these fields may allow for improved patient care and therapeutics based upon QSMs. Furthermore, bacterial whole-cell biosensors have elucidated the roles of some antibiotics as QS agonists and antagonists.
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References
Uroz S, Dessaux Y, Oger P (2009) Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chembiochem: Eur J Chem Biol 10(2):205–216. doi:10.1002/cbic.200800521
Gonzalez JE, Keshavan ND (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev: MMBR 70(4):859–875. doi:10.1128/MMBR.00002-06
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. doi:10.1146/annurev.cellbio.21.012704.131001
Kendall MM, Sperandio V (2014) Cell-to-cell signaling in and. EcoSal Plus 2014. doi:10.1128/ecosalplus.ESP-0002-2013
Sifri CD (2008) Healthcare epidemiology: quorum sensing: bacteria talk sense. Clin Infect Dis: Off Publ Infect Diseases Soc Am 47(8):1070–1076. doi:10.1086/592072
Sanchez CJ Jr, Mende K, Beckius ML, Akers KS, Romano DR, Wenke JC, Murray CK (2013) Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis 13:47. doi:10.1186/1471-2334-13-47
Raut N, O’Connor G, Pasini P, Daunert S (2012) Engineered cells as biosensing systems in biomedical analysis. Anal Bioanal Chem 402(10):3147–3159. doi:10.1007/s00216-012-5756-6
Cohen TP, D Prince A (2015) Host Immune Evasion. Pseudomonas 3–23. doi:10.1007/978-94-017-9555-5_1
Rumbaugh KP, Hamood AN, Griswold JA (2004) Cytokine induction by the P. aeruginosa quorum sensing system during thermal injury. The Journal of surgical research 116(1):137–144
Gjodsbol K, Christensen JJ, Karlsmark T, Jorgensen B, Klein BM, Krogfelt KA (2006) Multiple bacterial species reside in chronic wounds: a longitudinal study. Int Wound J 3(3):225–231. doi:10.1111/j.1742-481X.2006.00159.x
Kirketerp-Moller K, Jensen PO, Fazli M, Madsen KG, Pedersen J, Moser C, Tolker-Nielsen T, Hoiby N, Givskov M, Bjarnsholt T (2008) Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol 46(8):2717–2722. doi:10.1128/JCM.00501-08
Dalton T, Dowd SE, Wolcott RD, Sun Y, Watters C, Griswold JA, Rumbaugh KP (2011) An in vivo polymicrobial biofilm wound infection model to study interspecies interactions. PLoS ONE 6(11):e27317. doi:10.1371/journal.pone.0027317
Fekete A, Frommberger M, Rothballer M, Li X, Englmann M, Fekete J, Hartmann A, Eberl L, Schmitt-Kopplin P (2007) Identification of bacterial N-acylhomoserine lactones (AHLs) with a combination of ultra-performance liquid chromatography (UPLC), ultra-high-resolution mass spectrometry, and in-situ biosensors. Anal Bioanal Chem 387(2):455–467. doi:10.1007/s00216-006-0970-8
Struss AK, Nunes A, Waalen J, Lowery CA, Pullanikat P, Denery JR, Conrad DJ, Kaufmann GF, Janda KD (2013) Toward implementation of quorum sensing autoinducers as biomarkers for infectious disease states. Anal Chem 85(6):3355–3362. doi:10.1021/ac400032a
Kumari A, Pasini P, Daunert S (2008) Detection of bacterial quorum sensing N-acyl homoserine lactones in clinical samples. Anal Bioanal Chem 391(5):1619–1627. doi:10.1007/s00216-008-2002-3
Campagna SR, Gooding JR, May AL (2009) Direct quantitation of the quorum sensing signal, autoinducer-2, in clinically relevant samples by liquid chromatography-tandem mass spectrometry. Anal Chem 81(15):6374–6381. doi:10.1021/ac900824j
May AL, Eisenhauer ME, Coulston KS, Campagna SR (2012) Detection and quantitation of bacterial acylhomoserine lactone quorum sensing molecules via liquid chromatography-isotope dilution tandem mass spectrometry. Anal Chem 84(3):1243–1252. doi:10.1021/ac202636d
Ciofu O, Hansen CR, Hoiby N (2013) Respiratory bacterial infections in cystic fibrosis. Curr Opin Pulm Med 19(3):251–258. doi:10.1097/MCP.0b013e32835f1afc
Roy V, Meyer MT, Smith JA, Gamby S, Sintim HO, Ghodssi R, Bentley WE (2013) AI-2 analogs and antibiotics: a synergistic approach to reduce bacterial biofilms. Appl Microbiol Biotechnol 97(6):2627–2638. doi:10.1007/s00253-012-4404-6
Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407(6805):762–764. doi:10.1038/35037627
Bjarnsholt T (2013) The role of bacterial biofilms in chronic infections. APMIS Suppl 136:1–58. doi:10.1111/apm.12099
Middleton B, Rodgers HC, Camara M, Knox AJ, Williams P, Hardman A (2002) Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol Lett 207(1):1–7
Erickson DL, Endersby R, Kirkham A, Stuber K, Vollman DD, Rabin HR, Mitchell I, Storey DG (2002) Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun 70(4):1783–1790
Chambers CE, Visser MB, Schwab U, Sokol PA (2005) Identification of N-acylhomoserine lactones in mucopurulent respiratory secretions from cystic fibrosis patients. FEMS Microbiol Lett 244(2):297–304. doi:10.1016/j.femsle.2005.01.055
Sartor RB (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126(6):1620–1633
Kumari A, Pasini P, Deo SK, Flomenhoft D, Shashidhar H, Daunert S (2006) Biosensing systems for the detection of bacterial quorum signaling molecules. Anal Chem 78(22):7603–7609. doi:10.1021/ac061421n
Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GS (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163(2):185–192
Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Camara M, Smith H, Williams P (2002) N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70(10):5635–5646
Yang F, Wang LH, Wang J, Dong YH, Hu JY, Zhang LH (2005) Quorum quenching enzyme activity is widely conserved in the sera of mammalian species. FEBS Lett 579(17):3713–3717. doi:10.1016/j.febslet.2005.05.060
Raut N, Pasini P, Daunert S (2013) Deciphering bacterial universal language by detecting the quorum sensing signal, autoinducer-2, with a whole-cell sensing system. Anal Chem 85(20):9604–9609. doi:10.1021/ac401776k
Kumar R, Chhibber S, Gupta V, Harjai K (2011) Screening & profiling of quorum sensing signal molecules in Pseudomonas aeruginosa isolates from catheterized urinary tract infection patients. Ind J Med Res 134:208–213
Senturk S, Ulusoy S, Bosgelmez-Tinaz G, Yagci A (2012) Quorum sensing and virulence of Pseudomonas aeruginosa during urinary tract infections. J Infect Dev Countries 6(6):501–507
Lakshmana Gowda K, John J, Marie MA, Sangeetha G, Bindurani SR (2013) Isolation and characterization of quorum-sensing signalling molecules in Pseudomonas aeruginosa isolates recovered from nosocomial infections. APMIS: Acta Pathol Microbiol Immunol Scand. doi:10.1111/apm.12047
Gupta P, Gupta RK, Harjai K (2013) Quorum sensing signal molecules produced by Pseudomonas aeruginosa cause inflammation and escape host factors in murine model of urinary tract infection. Inflammation 36(5):1153–1159. doi:10.1007/s10753-013-9650-y
Daunert S, Barrett G, Feliciano JS, Shetty RS, Shrestha S, Smith-Spencer W (2000) Genetically engineered whole-cell sensing systems: coupling biological recognition with reporter genes. Chem Rev 100(7):2705–2738
Feliciano JP, Deo P, Daunert, S (2006) Photoproteins as reporters in whole-cell sensing. Wiley-VCH Verlag GmbH & Co KGaA 131–154
Yong YC, Zhong JJ (2009) A genetically engineered whole-cell pigment-based bacterial biosensing system for quantification of N-butyryl homoserine lactone quorum sensing signal. Biosens Bioelectron 25(1):41–47. doi:10.1016/j.bios.2009.06.010
Struss A, Pasini P, Ensor CM, Raut N, Daunert S (2010) Paper strip whole cell biosensors: a portable test for the semiquantitative detection of bacterial quorum signaling molecules. Anal Chem 82(11):4457–4463. doi:10.1021/ac100231a
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199. doi:10.1146/annurev.micro.55.1.165
Federle MJ (2009) Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling. Contrib Microbiol 16:18–32. doi:10.1159/000219371
Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of faecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55(2):205–211. doi:10.1136/gut.2005.073817
Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedmann M, McDonough P, Kim SG, Berg D, Schukken Y, Scherl E, Simpson KW (2007) Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn’s disease involving the ileum. ISME J 1(5):403–418. doi:10.1038/ismej.2007.52
Swift S, Throup JP, Williams P, Salmond GP, Stewart GS (1996) Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends Biochem Sci 21(6):214–219
Reverchon S, Chantegrel B, Deshayes C, Doutheau A, Cotte-Pattat N (2002) New synthetic analogues of N-acyl homoserine lactones as agonists or antagonists of transcriptional regulators involved in bacterial quorum sensing. Bioorg Med Chem Lett 12(8):1153–1157
Kai T, Tateda K, Kimura S, Ishii Y, Ito H, Yoshida H, Kimura T, Yamaguchi K (2009) A low concentration of azithromycin inhibits the mRNA expression of N-acyl homoserine lactone synthesis enzymes, upstream of lasI or rhlI, in Pseudomonas aeruginosa. Pulm Pharmacol Ther 22(6):483–486. doi:10.1016/j.pupt.2009.04.004
Struss AK, Pasini P, Flomenhoft D, Shashidhar H, Daunert S (2012) Investigating the effect of antibiotics on quorum sensing with whole-cell biosensing systems. Anal Bioanal Chem 402(10):3227–3236. doi:10.1007/s00216-012-5710-7
Gillis RJ, Iglewski BH (2004) Azithromycin retards Pseudomonas aeruginosa biofilm formation. J Clin Microbiol 42(12):5842–5845. doi:10.1128/JCM.42.12.5842-5845.2004
Nalca Y, Jansch L, Bredenbruch F, Geffers, R, Buer J, Haussler S (2006) Quorum-Sensing Antagonistic Activities of Azithromycin in Pseudomonas aeruginosa PAO1: a Global Approach. Antimicrob. Agents Chemother 50:1680–1668
Bala A, Kumar R, Harjai K (2011) Inhibition of quorum sensing in Pseudomonas aeruginosa by azithromycin and its effectiveness in urinary tract infections. J Med Microbiol 60(Pt 3):300–306. doi:10.1099/jmm.0.025387-0
Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB, Bjarnsholt T, Tolker-Nielsen T, Hoiby N, Givskov M (2008) Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52(10):3648–3663. doi:10.1128/AAC.01230-07
Bottomley MJ, Muraglia E, Bazzo R, Carfi 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(18):13592–13600. doi:10.1074/jbc.M700556200
Raut N, Joel S, Pasini P, Daunert S (2015) Bacterial autoinducer-2 detection via an engineered quorum sensing protein. Anal Chem 87(5):2608–2614. doi:10.1021/ac504172f
Scharff RL (2012) Economic burden from health losses due to foodborne illness in the United States. J Food Prot 75(1):123–131. doi:10.4315/0362-028X.JFP-11-058
Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM (2011) Foodborne illness acquired in the United States–unspecified agents. Emerg Infect Dis 17(1):16–22. doi:10.3201/eid1701.091101p2
Skandamis PN, Nychas GJ (2012) Quorum sensing in the context of food microbiology. Appl Environ Microbiol 78(16):5473–5482. doi:10.1128/AEM.00468-12
DeAngelis KM, Firestone MK, Lindow SE (2007) Sensitive whole-cell biosensor suitable for detecting a variety of N-acyl homoserine lactones in intact rhizosphere microbial communities. Appl Environ Microbiol 73(11):3724–3727. doi:10.1128/AEM.02187-06
Burmolle M, Hansen LH, Sorensen SJ (2005) Use of a whole-cell biosensor and flow cytometry to detect AHL production by an indigenous soil community during decomposition of litter. Microb Ecol 50(2):221–229. doi:10.1007/s00248-004-0113-8
Michael B, Smith JN, Swift S, Heffron F, Ahmer BM (2001) SdiA of Salmonella enterica is a LuxR homolog that detects mixed microbial communities. J Bacteriol 183(19):5733–5742. doi:10.1128/JB.183.19.5733-5742.2001
Smith JN, Ahmer BM (2003) Detection of other microbial species by Salmonella: expression of the SdiA regulon. J Bacteriol 185(4):1357–1366
Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V (2006) The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci USA 103(27):10420–10425. doi:10.1073/pnas.0604343103
Crabbe A, Sarker SF, Van Houdt R, Ott CM, Leys N, Cornelis P, Nickerson CA (2011) Alveolar epithelium protects macrophages from quorum sensing-induced cytotoxicity in a three-dimensional co-culture model. Cell Microbiol 13(3):469–481. doi:10.1111/j.1462-5822.2010.01548.x
Acknowledgments
This work was supported in part by grants from the National Science Foundation, the Broad Foundation, Broad Medical Research Program, National Institute of Hometown Security, the Children’s Miracle Network, and the Department of Defense. S.D. is grateful for support from the Lucille P. Markey Chair in Biochemistry and Molecular Biology of the Miller School of Medicine of the University of Miami.
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O’Connor, G., Knecht, L.D., Salgado, N., Strobel, S., Pasini, P., Daunert, S. (2015). Whole-Cell Biosensors as Tools for the Detection of Quorum-Sensing Molecules: Uses in Diagnostics and the Investigation of the Quorum-Sensing Mechanism. In: Thouand, G., Marks, R. (eds) Bioluminescence: Fundamentals and Applications in Biotechnology - Volume 3. Advances in Biochemical Engineering/Biotechnology, vol 154. Springer, Cham. https://doi.org/10.1007/10_2015_337
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