Skip to main content
Log in

Mathematical Modelling of Bacterial Quorum Sensing: A Review

  • Review Article
  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

Bacterial quorum sensing (QS) refers to the process of cell-to-cell bacterial communication enabled through the production and sensing of the local concentration of small molecules called autoinducers to regulate the production of gene products (e.g. enzymes or virulence factors). Through autoinducers, bacteria interact with individuals of the same species, other bacterial species, and with their host. Among QS-regulated processes mediated through autoinducers are aggregation, biofilm formation, bioluminescence, and sporulation. Autoinducers are therefore “master” regulators of bacterial lifestyles. For over 10 years, mathematical modelling of QS has sought, in parallel to experimental discoveries, to elucidate the mechanisms regulating this process. In this review, we present the progress in mathematical modelling of QS, highlighting the various theoretical approaches that have been used and discussing some of the insights that have emerged. Modelling of QS has benefited almost from the onset of the involvement of experimentalists, with many of the papers which we review, published in non-mathematical journals. This review therefore attempts to give a broad overview of the topic to the mathematical biology community, as well as the current modelling efforts and future challenges.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

Notes

  1. A mathematical framework was used before to address QS in the context of evolution, see Sect. 2.4.

References

  • Almeida AR, Amado IF, Reynolds J, Berges J, Lythe G, Molina-Paris C, Freitas AA (2012) Quorum sensing in CD4\(+\) T cell homoeostasis: a hypothesis and a model. Front. Immunol. 3. doi:10.3389/fimmu.2012.00125

  • Anand R, Rai N, Thattai M (2013) Interactions among quorum sensing inhibitors. PLOS One 8:e62254

    Article  Google Scholar 

  • Anetzberger C, Pirch T, Jung K (2009) Heterogeneity in quorum sensing-regulated bioluminescence of Vibrio harveyi. Mol Microbiol 73:267–277. doi:10.1111/j.1365-2958.2009.06768.x

    Article  Google Scholar 

  • Anguige K, King JR, Ward JP (2005) Modelling antibiotic- and anti-quorum sensing treatment of a spatially-structured Pseudomonas aeruginosa population. J Math Biol 51(5):557–594. doi:10.1007/s00285-005-0316-8

    Article  MathSciNet  MATH  Google Scholar 

  • Anguige K, King JR, Ward JP (2006) A multi-phase mathematical model of quorum sensing in a maturing Pseudomonas aeruginosa biofilm. Math Biosci 203:240–276. doi:10.1016/j.mbs.2006.05.009

    Article  MathSciNet  MATH  Google Scholar 

  • Anguige K, King JR, Ward JP, Williams P (2004) Mathematical modelling of therapies targeted at bacterial quorum sensing. Math Biosci 192(1):39–83. doi:10.1016/j.mbs.2004.06.008

    Article  MathSciNet  MATH  Google Scholar 

  • Banik SK, Fenley AT, Kulkarni RV (2009) A model for signal transduction during quorum sensing in Vibrio harveyi. Phys Biol 6. doi:10.1088/1478-3975/6/4/046008

  • Barbarossa M, Kuttler C, Fekete A, Rothballer M (2010) A delay model for quorum sensing of Pseudomonas putida. Biosystems 102:148–156. doi:10.1016/j.biosystems.2010.09.001

    Article  Google Scholar 

  • Beckmann BE, Knoester DB, Connelly BD, Waters CM, McKinley PK (2012) Evolution of resistance to quorum quenching in digital organisms. Artif Life 18:291–310. doi:10.1162/artl_a_00066

  • Ben-Jacob E, Cohen I, Levine H (2000) Cooperative self-organization of microorganisms. Adv Phys 49:395–554. doi:10.1080/000187300405228

    Article  Google Scholar 

  • Bischofs IB, Hug JA, Liu AW, Wolf DM, Arkin AP (2009) Complexity in bacterial cell-cell communication: quorum signal integration and subpopulation signaling in the Bacillus subtilis phosphorelay. Proc Natl Acad Sci USA 106:6459–6464. doi:10.1073/pnas.0810878106

    Article  Google Scholar 

  • Boyer M, Wisniewski-Dyé F (2009) Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 70:1–9. doi:10.1111/j.1574-6941.2009.00745.x

    Article  Google Scholar 

  • Boedicker J, Vincent M, Ismagilov R (2009) Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew Chem Int Ed 48:5908–5911. doi:10.1002/anie.200901550

    Article  Google Scholar 

  • Brookfield J (1998) Quorum sensing and group selection. Evolution 52:1263–1269

    Article  Google Scholar 

  • Brown D (2010) A mathematical model of the gac/rsm quorum sensing network in Pseudomonas fluorescens. Biosystems 101:200–212. doi:10.1016/j.biosystems.2010.07.004

    Article  Google Scholar 

  • Brown D (2013) Linking molecular and population processes in mathematical models of quorum sensing. Bull Math Biol 75:1813–1839. doi:10.1007/s11538-013-9870-1

    Article  MathSciNet  MATH  Google Scholar 

  • Brown SP (1999) Cooperation and conflict in host-manipulating parasites. Proc R Soc B 266:1899–1899. doi:10.1098/rspb.1999.0864

    Article  Google Scholar 

  • Brown SP, Johnstone RA (2001) Cooperation in the dark: signalling and collective action in quorum-sensing bacteria. Proc R Soc B 268:961–965. doi:10.1098/rspb.2001.1609

    Article  Google Scholar 

  • Brown SP, West SA, Diggle SP, Griffin AS (2009) Social evolution in micro-organisms and a trojan horse approach to medical intervention strategies. Philos Trans R Soc B 364:3157–3168. doi:10.1098/rstb.2009.0055

    Article  Google Scholar 

  • Busby S, de Lorenzo V (2001) Cell regulation: putting together pieces of the big puzzle. Curr Opin Microbiol 4:117–118. doi:10.1016/S1369-5274(00)00175-2

    Article  Google Scholar 

  • Calfee MW, Coleman JP, Pesci EC (2001) Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 98:11633–11637

    Article  Google Scholar 

  • Carnes EC, Lopez DM, Donegan NP, Cheung A, Gresham H, Timmins GS, Brinker (2010) Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat Chem Biol 6, 41–45. URL: http://www.ncbi.nlm.nih.gov/pubmed/19935660

  • Castillo-Juarez I, Maeda T, Mandujano-Tinoco EA, Tomas M, Perez-Eretza B, Garcia-Contreras R (2015) Role of quorum sensing in bacterial infections. World J Clin Cases 3:575–598

    Google Scholar 

  • Chen CC, Riadi L, Suh SJ, Ohman DE, Ju LK (2005) Degradation and synthesis kinetics of quorum-sensing autoinducer in Pseudomonas aeruginosa cultivation. J Biotechnol 117:1–10. doi:10.1016/j.jbiotec.2005.01.003

    Article  Google Scholar 

  • Chen F, Chen CC, Riadi L, Ju LK (2004) Role of quorum sensing in bacterial infections. Biotechnol Prog 20:1325–1331. doi:10.1021/bp049928b

    Article  Google Scholar 

  • Chen MT, Weiss R (2005) Artificial cell-cell communication in yeast Saccharomyces cerevisiae using signaling elements from Arabidopsis thaliana. Nat Biotechnol 23:1551–1555. doi:10.1038/nbt1162

    Article  Google Scholar 

  • Chopp DL, Kirisits MJ, Moran B, Parsek MR (2002a) The dependence of quorum sensing on the depth of a growing biofilm. Bull Math Biol 65:1053–1079

    Article  MATH  Google Scholar 

  • Chopp DL, Kirisits MJ, Moran B, Parsek MR (2002b) A mathematical model for quorum sensing in a growing bacterial biofilm. J Ind Microbiol Biotechnol 296:339–346

    Article  MATH  Google Scholar 

  • Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci USA 111:4280–4284. doi:10.1073/pnas.1319175111

    Article  Google Scholar 

  • Costerton JW, Stewart P, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322

    Article  Google Scholar 

  • Cox CD, Peterson GD, Allen MS, Lancaster JM, McCollum JM, Austin D, Yan L, Sayler GS, Simpson ML (2003) Analysis of noise in quorum sensing. OMICS 7:317–334. doi:10.1089/153623103322452422

    Article  Google Scholar 

  • Czárán T, Hoekstra RF (2009) Microbial communication, cooperation and cheating: Quorum sensing drives the evolution of cooperation in bacteria. PLoS One 4:e6655. doi:10.1371/journal.pone.0006655

    Article  Google Scholar 

  • Damore JA, Gore J (2012) Understanding microbial cooperation. J Theor Biol 299:31–41. doi:10.1016/j.jtbi.2011.03.008

    Article  MathSciNet  MATH  Google Scholar 

  • Danino T, Mondragon-Palomino O, Tsimring L, Hasty J (2010) A synchronized quorum of genetic clocks. Nature 463:326–330. doi:10.1038/nature08753

    Article  Google Scholar 

  • Davies DSC (2011) Annual report of the chief medical officer. Technical Report. British Department of Health

  • Dilanji GE, Langebrake JB, De Leenheer P, Hagen SJ (2012) Quorum activation at a distance: spatiotemporal patterns of gene regulation from diffusion of an autoinducer signal. J Am Chem Soc 134:5618–5626. doi:10.1021/ja211593q

    Article  Google Scholar 

  • Dockery J, Keener J (2001) A mathematical model for quorum sensing in Pseudomonas aeruginosa. Bull Math Biol 63:95–116. doi:10.1006/bulm.2000.0205

    Article  MATH  Google Scholar 

  • Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759. doi:10.1128/AEM.68.4.1754-1759.2002

    Article  Google Scholar 

  • Duddu R, Chopp DL, Moran B (2009) A two-dimensional continuum model of biofilm growth incorporating fluid flow and shear stress based detachment. Biotechnol Bioeng 103:92–104. doi:10.1002/bit.22233

    Article  Google Scholar 

  • Dumas Z, Ross-Gillespie A, Kmmerli R (2013) Switching between apparently redundant iron-uptake mechanisms benefits bacteria in changeable environments. Proc R Soc B 280. doi:10.1098/rspb.2013.1055

  • Eberl H, Parker D, van Loosdrecht M (2001) A new deterministic spatio-temporal continuum model for biofilm development. J Theor Med 3:161–175. doi:10.1080/10273660108833072

    Article  MATH  Google Scholar 

  • Eberl H, Morgenroth E, Noguera D, Picioreanu C, Rittmann B, van Loosdrecht M, Wanner O (2006) Mathematical modeling of biofilms. Scientific and technical report, IWA Publishing. URL: https://books.google.de/books?id=hRsRy6jSKKAC

  • Fagerlind MG, Nilsson P, Harlén M, Karlsson S, Rice SA, Kjelleberg S (2005) Modeling the effect of acylated homoserine lactone antagonists in Pseudomonas aeruginosa. Biosystems 80:201–213. doi:10.1016/j.biosystems.2004.11.008

    Article  Google Scholar 

  • Fagerlind MG, Rice SA, Nilsson P, Harlén M, James S, Charlton T, Kjelleberg S (2003) The role of regulators in the expression of quorum-sensing signals in Pseudomonas aeruginosa. J Mol Microbiol Biotechnol 6:88–100. doi: 10.1159/000076739

  • Fekete A, Kuttler C, Rothballer M, Hense BA, Fischer D, Buddrus-Schiemann K, Lucio M, Müller J, Schmitt-Kopplin P, Hartmann A (2010) Dynamic regulation of n-acyl-homoserine lactone production and degradation in Pseudomonas putida ISOF. FEMS Microbiol Ecol 72:22–34. doi:10.1111/j.1574-6941.2009.00828.x

    Article  Google Scholar 

  • Fenley AT, Banik SK, Kulkarni RV (2011) Computational modeling of differences in the quorum sensing induced luminescence phenotypes of Vibrio harveyi and Vibrio cholerae. J Theor Biol 274(1):145–153. doi:10.1016/j.jtbi.2011.01.008

    Article  Google Scholar 

  • Fletcher JA, Doebeli M (2009) A simple and general explanation for the evolution of altruism. Proc R Soc B 276:13–19

    Article  Google Scholar 

  • Fozard J, Lees M, King J, Logan B (2012) Inhibition of quorum sensing in a computational biofilm simulation. Biosystems 109:105–114. doi:10.1016/j.biosystems.2012.02.002

    Article  Google Scholar 

  • Frederick M, Kuttler C, Hense B, Müller J, Eberl H (2010) A mathematical model of quorum sensing in patchy biofilm communities with slow background flow. Can Appl Math Q 18:267–298

    MathSciNet  MATH  Google Scholar 

  • Frederick MR, Kuttler C, Hense BA, Eberl HJ (2011) A mathematical model of quorum sensing regulated eps production in biofilm communities. Theor Biol Med Model. 8. doi:10.1186/1742-4682-8-8

  • Friman VP, Diggle SP, Buckling A (2013) Protist predation can favour cooperation within bacterial species. Biol Lett 9. doi:10.1098/rsbl.2013.0548

  • Friman VP, Ghoul M, Molin S, Johansen HK, Buckling A (2013b) Pseudomonas aeruginosa adaptation to lungs of cystic fibrosis patients leads to lowered resistance to phage and protist enemies. PLoS One 8:e75380. doi:10.1371/journal.pone.0075380

    Article  Google Scholar 

  • Fujimoto K, Sawai S (2013) A design principle of group-level decision making in cell populations. PLoS Comput Biol 9:e1003110. doi:10.1371/journal.pcbi.1003110

    Article  Google Scholar 

  • Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria - the luxr-luxi family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

    Google Scholar 

  • Galloway WR, Hodgkinson JT, Bowden S, Welch M, Spring DR (2012) Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria. Trends Microbiol 20:449–458. doi:10.1016/j.tim.2012.06.003

    Article  Google Scholar 

  • García-Contreras R, Maeda T, Wood TK (2013) Resistance to quorum-quenching compounds. Appl Environ Microbiol 79:6840–6846. doi:10.1128/AEM.02378-13

    Article  Google Scholar 

  • García-Contreras R, Maeda T, Wood TK (2015) Can resistance against quorum-sensing interference be selected?. ISME J 1751–7370. URL: http://www.nature.com/ismej/journal/vaop/ncurrent/full/ismej201584a.html

  • García-Contreras R, Nunez-Lopez L, Jasso-Chavez R, Kwan BW, Belmont JA, Rangel-Vega A, Maeda T, Wood TK (2015) Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J 9:115–125. doi:10.1038/ismej.2014.98

    Article  Google Scholar 

  • García-Ojalvo J, Elowitz MB, Strogatz SH (2004) Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. Proc Natl Acad Sci USA 101:10955–10960. doi:10.1073/pnas.0307095101

    Article  MathSciNet  MATH  Google Scholar 

  • Gillespie DT (1977) Exact stochastic simulation of coupled chemical reactions. J Phys Chem A 81:2340–2361. doi:10.1021/j100540a008

    Article  Google Scholar 

  • Gölgeli Matur M, Müller J, Kuttler C, Hense BA (2014) An approximative approach for single cell spatial modeling of quorum sensing. J Comput Biol. doi:10.1089/cmb.2014.0198

  • González-Barrios AF, Covo V, Medina LM, Vives-Florez M, Achenie L (2009) Quorum quenching analysis in Pseudomonas aeruginosa and Escherichia coli: network topology and inhibition mechanism effect on the optimized inhibitor dose. Bioprocess Biosyst Eng 32:545–556. doi:10.1007/s00449-008-0276-7

    Article  Google Scholar 

  • González-Barrios AF, Achenie LE (2010) Escherichia coli autoinducer-2 uptake network does not display hysteretic behavior but ai-2 synthesis rate controls transient bifurcation. Biosystems 99:17–26. doi:10.1016/j.biosystems.2009.08.003

    Article  Google Scholar 

  • Goryachev AB (2009) Design principles of the bacterial quorum sensing gene networks. Wiley Interdiscip Rev Syst Biol Med 1:45–60. doi:10.1002/wsbm.27

    Article  Google Scholar 

  • Goryachev AB (2011) Understanding bacterial cell-cell communication with computational modeling. Chem Rev 111:238–250. doi:10.1021/cr100286z

    Article  Google Scholar 

  • Goryachev AB, Toh DJ, Lee T (2006) Systems analysis of a quorum sensing network: Design constraints imposed by the functional requirements, network topology and kinetic constants. BioSystems 83: 178–187. URL: http://goryachev.bio.ed.ac.uk/goryachev/sites/sbsweb2.bio.ed.ac.uk.goryachev/files/pdf/BioSys0206

  • Goryachev AB, Toh DJ, Wee KB, Lee T, Zhang HB, Zhang LH (2005) Transition to quorum sensing in an agrobacterium population: a stochastic model. PLoS Comput Biol 1(4):e37. doi:10.1371/journal.pcbi.0010037

    Article  Google Scholar 

  • Goss PJE, Peccoud J (1998) Quantitative modeling of stochastic systems in molecular biology by using stochastic petri nets. Proc Natl Acad Sci USA 95:6750–6755. URL: http://www.pnas.org/content/95/12/6750.abstract

  • Gupta P, Chhibber S, Harjai K (2015) Efficacy of purified lactonase and ciprofloxacin in preventing systemic spread of Pseudomonas aeruginosa in murine burn wound model. Burns 41:153–162

    Article  Google Scholar 

  • Gustafsson E, Nilsson P, Karlsson S, Arvidson S (2004) Characterizing the dynamics of the quorum-sensing system in Staphylococcus aureus. J Mol Microbiol Biotechnol 8:232–242. doi: 10.1159/000086704

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–16

    Article  Google Scholar 

  • Haseltine EL, Arnold FH (2008) Implications of rewiring bacterial quorum sensing. Appl Environ Microbiol 74:437–445

    Article  Google Scholar 

  • Hastings JW, Nealson KH (1977) Bacterial bioluminescence. Annu Rev Microbiol 31:549–595. doi:10.1146/annurev.mi.31.100177.003001

    Article  Google Scholar 

  • Hense BA, Kuttler C, Müller J, Rothballer M, Hartmann A, Kreft JU (2007) Does efficiency sensing unify diffusion and quorum sensing? Nat Rev Microbiol 5:230–239. doi:10.1038/nrmicro1600

    Article  Google Scholar 

  • Hense BA, Müller J, Kuttler C, Hartmann A (2012) Spatial heterogeneity of autoinducer regulation systems. Sensors 12(4):4156–4171. doi:10.3390/s120404156

    Article  Google Scholar 

  • Hense BA, Schuster M (2015) Core principles of bacterial autoinducer systems. Microbiol Mol Biol Rev 79:153–169. doi:10.1128/MMBR.00024-14

    Article  Google Scholar 

  • Hong D, Saidel WM, Man S, Martin JV (2007) Extracellular noise-induced stochastic synchronization in heterogeneous quorum sensing network. J Theor Biol 245:726–736. URL: http://www.sciencedirect.com/science/article/pii/S0022519306005662

  • Hunter GAM, Vasquez FG, Keener JP (2013) A mathematical model and quantitative comparison of the small RNA circuit in the Vibrio harveyi and Vibrio cholerae quorum sensing systems. Phys Biol 10:046007. URL: http://stacks.iop.org/1478-3975/10/i=4/a=046007

  • Jabbari S, King JR, Koerber AJ, Williams P (2010) Mathematical modelling of the agr operon in Staphylococcus aureus. J Math Biol 61:17–54

    Article  MathSciNet  MATH  Google Scholar 

  • James S, Nilsson P, James G, Kjelleberg S, Fagersötrm T (2000) Luminescence control in the marine bacterium Vibrio fischeri: an analysis of the dynamics of lux regulation. J Mol Biol 296:1127–1137. doi:10.1006/jmbi.1999.3484

    Article  Google Scholar 

  • Janakiramen V, Englert D, Jayaman A, Baskaran H (2009) Modeling growth and quorum sensing in biofilms grown in microfluidic chambers. Ann Biomed Eng 37:1206–1216

    Article  Google Scholar 

  • Joyner DC, Lindow SE (2000) Heterogeneity of iron bioavailability on plants assessed with a whole-cell GFP-based bacterial biosensor. Microbiology 146:2435–2445. URL: http://mic.sgmjournals.org/content/146/10/2435.abstract

  • Kaplan HB, Greenberg EP (1985) Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system. J Bacteriol 163:1210–1214. URL: http://jb.asm.org/content/163/3/1210.abstract

  • Kang Y, Saile E, Schell MA, Denny TP (1999) Quantitative immunofluorescence of regulated EPS gene expression in single cells of Ralstonia solanacearum. Appl Environ Microbiol 65:2356–2362. URL: http://aem.asm.org/content/65/6/2356.abstract

  • Karlsson D, Karlsson S, Gustafsson E, Normark BH, Nilsson P (2007) Modeling the regulation of the competence-evoking quorum sensing network in Streptococcus pneumoniae. BioSystems 90:211–223

    Article  Google Scholar 

  • Kirisits MJ, Margolis JJ, Purevdorj-Gage BL, Vaughan B, Chopp DL, Stoodley P, Parsek MR (2007) Influence of the hydrodynamic environment on quorum sensing in Pseudomonas aeruginosa biofilms. J Bacteriol 189:8357–8360. doi:10.1128/JB.01040-07

    Article  Google Scholar 

  • Klapper I, Dockery J (2010) Mathematical description of microbial biofilms. SIAM Rev 52:000–000

    Article  MathSciNet  MATH  Google Scholar 

  • Koerber A, King J, Ward J, Williams P, Croft J, Sockett R (2002) A mathematical model of partial-thickness burn-wound infection by Pseudomonas aeruginosa: quorum sensing and the build-up to invasion. Bull Math Biol 64:239–259. doi:10.1006/bulm.2001.0272

    Article  MATH  Google Scholar 

  • Koerber AJ, King JR, Williams P (2005) Deterministic and stochastic modelling of endosome escape by Staphylococcus aureus: quorum sensing by a single bacterium. J Math Biol 50(4):440–488. doi:10.1007/s00285-004-0296-0

    Article  MathSciNet  MATH  Google Scholar 

  • Koseska A, Volkov E, Zaikin A, Kurths J (2007) Quantized cycling time in artificial gene networks induced by noise and intercell communication. Phys Rev E 76:020901. doi:10.1103/PhysRevE.76.020901

    Article  Google Scholar 

  • Kumar S, Kolodkin-Gal I, Engelberg-Kulka H (2013) Novel quorum sensing peptides mediating interspecies bacterial cell death. MBio 4(3):e00314-13. doi:10.1128/mBio.00314-13

    Article  Google Scholar 

  • Kuttler C, Hense BA (2008) Interplay of two quorum sensing regulation systems of Vibrio fischeri. J Theor Biol 251:167–180. doi:10.1016/j.jtbi.2007.11.015

    Article  MathSciNet  Google Scholar 

  • Kuznetsov A, Krn M, Kopell N (2004) Synchrony in a population of hysteresis-based genetic oscillators. SIAM J Appl Math 65

  • Langebrake JB, Dilanji GE, Hagen SJ, Leenheer PD (2014) Traveling waves in response to a diffusing quorum sensing signal in spatially-extended bacterial colonies. J Theor Biol 363:53–61. doi:10.1016/j.jtbi.2014.07.033

    Article  MathSciNet  MATH  Google Scholar 

  • Lazdunski AM, Ventre I, Sturgis JN (2004) Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2:581–592

    Article  Google Scholar 

  • Lee J, Jayaraman A, Wood TK (2007) Indole is an inter-species biofilm signal mediated by SdiA. Microbiol 7:42. doi:10.1186/1471-2180-7-42

    Google Scholar 

  • Lesic B, de Lorenzo V, Lepine F, Deziel E, Zhang J, Zhang Q, Padfield K (2007) Inhibitors of pathogen intercellular signals as selective anti-infective compounds. PLoS Pathog 3:1229–1239

    Article  Google Scholar 

  • Li J, Wang L, Hashimoto Y, Tsao CY, Wood TK, Valdes JJ, Zafiriou E, Bentley WE (2006) A stochastic model of Escherichia coli ai-2 quorum signal circuit reveals alternative synthesis pathways. Mol Syst Biol 2. doi:10.1038/msb4100107

  • Liu X, Zhou P, Wang R (2012) Switch-like regulation of signal transduction by small RNA-mediated quorum sensing. In: 2012 IEEE 6th international conference on systems biology (ISB), pp 164–168. doi:10.1109/ISB.2012.6314130

  • Liu X, Zhou P, Wang R (2013) Small rna-mediated switch-like regulation in bacterial quorum sensing. IET Syst Biol 7:182–187. doi:10.1049/iet-syb.2012.0059

    Article  MathSciNet  Google Scholar 

  • Lyon GJ, Novick RP (2004) Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25:1389–1403

    Article  Google Scholar 

  • Maeda T, García-Contreras R, Pu M, Sheng L, García LR, Tomas M, Wood TK (2012) Quorum quenching quandary: resistance to antivirulence compounds. ISME J 6:493–501. doi:10.1038/ismej.2011.122

    Article  Google Scholar 

  • Majumdar S, Datta S, Roy S (2012) Mathematical modelling of quorum sensing and bioluminescence in bacteria. IJAAS 1(3):139–146

    Google Scholar 

  • McMillen D, Kopell N, Hasty J, Collins JJ (2002) Synchronizing genetic relaxation oscillators by intercell signaling. Proc Natl Acad Sci USA 99:679–684. doi:10.1073/pnas.022642299

    Article  Google Scholar 

  • Mehra S, Charaniya S, Takano E, Hu WS (2008) A bistable gene switch for antibiotic biosynthesis: the butyrolactone regulon in Streptomyces coelicolor. PLoS One 3:e2724. doi:10.1371/journal.pone.0002724

    Article  Google Scholar 

  • Mehta P, Goyal S, Long T, Bassler BL, Wingreen NS (2009) Information processing and signal integration in bacterial quorum sensing. Mol Syst Biol 5. doi:10.1038/msb.2009.79

  • Melke P, Sahlin P, Levchenko A, Jönsson H (2010) A cell-based model for quorum sensing in heterogeneous bacterial colonies. PLoS Comput Biol 6(6):e1000819

    Article  MathSciNet  Google Scholar 

  • Megerle JA, Fritz G, Gerland U, Jung K, Rädler JO (2008) Timing and dynamics of single cell gene expression in the Arabinose utilization system. Biophys J 95: 2103–2115. URL: http://linkinghub.elsevier.com/retrieve/pii/S0006349508701681

  • Meyer A, Megerle JA, Kuttler C, Müller J, Aguilar C, Eberl L, Hense BA, Rädler JO (2012) Dynamics of ahl mediated quorum sensing under flow and non-flow conditions. Phys Biol 9: 026007. URL: http://stacks.iop.org/1478-3975/9/i=2/a=026007

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199. doi:10.1146/annurev.micro.55.1.165

    Article  Google Scholar 

  • Müller J, Kuttler C, Hense BA (2008a) Sensitivity of the quorum sensing system is achieved by low pass filtering. Biosystems 92:76–81. doi:10.1016/j.biosystems.2007.12.004

    Article  Google Scholar 

  • Müller J, Kuttler C, Hense BA, Rothballer M, Hartmann A (2006) Cell-cell communication by quorum sensing and dimension-reduction. J Math Biol 53:672–702. doi:10.1007/s00285-006-0024-z

    Article  MathSciNet  MATH  Google Scholar 

  • Müller J, Kuttler C, Hense BA, Zeiser S, Liebscher V (2008) Transcription, intercellular variability and correlated random walk. Math Biosci 216:30–39. doi:10.1016/j.mbs.2008.08.003

    Article  MathSciNet  MATH  Google Scholar 

  • Müller J, Uecker H (2013) Approximating the dynamics of communicating cells in a diffusive medium by odeshomogenization with localization. J Math Biol 67:1023–1065. doi:10.1007/s00285-012-0569-y

    Article  MathSciNet  MATH  Google Scholar 

  • Nadell CD, Xavier JB, Levin SA, Foster KR (2008) The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6:e14. doi:10.1371/journal.pbio.0060014

    Article  Google Scholar 

  • Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43:496–518. URL: http://mmbr.asm.org/content/43/4/496.short

  • Netotea S, Bertani I, Steindler L, Kerényi Á, Venturi V, Pongor S (2009) A simple model for the early events of quorum sensing in Pseudomonas aeruginosa: modeling bacterial swarming as the movement of an “activation zone”. Biol Direct 4:6–6. doi:10.1186/1745-6150-4-6

    Article  Google Scholar 

  • Nilsson P, Olofsson A, Fagerlind M, Fagerström T, Rice S, Kjelleberg S, Steinberg P (2001) Kinetics of the ahl regulatory system in a model biofilm system: how many bacteria constitute a “quorum”? J Mol Biol 309(3):631–640. doi:10.1006/jmbi.2001.4697

    Article  Google Scholar 

  • Ofria C, Wilke CO (2004) Avida: A software platform for research in computational evolutionary biology. Artif Life 10:191–229. doi:10.1162/106454604773563612

    Article  Google Scholar 

  • O’Loughlin CT, Miller LC, Siryaporn A, Drescher K, Semmelhack MF, Bassler BL (2013) A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci USA 110:17981–17986

    Article  Google Scholar 

  • Palmer KL, Aye LM, Whiteley M (2007) Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J Bacteriol 189:8079–8087

    Article  Google Scholar 

  • Perez P, Weiss J, Hagen S (2011) Noise and crosstalk in two quorum-sensing inputs of Vibrio fischeri. BMC Syst Biol 5:153. doi:10.1186/1752-0509-5-153

    Article  Google Scholar 

  • Pérez-Jiménez MJ, Romero-Campero FJ (2006) P systems, a new computational modelling tool for systems biology. In: Priami C, Plotkin G (eds) Transactions on computational systems biology VI, vol. 4220 of Lecture Notes in Computer Science, Springer, Berlin, pp 176–197. doi:10.1007/11880646_8

  • Pérez-Velázquez J, Quiñones B, Hense BA, Kuttler C (2015) A mathematical model to investigate quorum sensing regulation and its heterogeneity in Pseudomonas syringae on leaves. Ecol Complex 21:128–141. doi:10.1016/j.ecocom.2014.12.003

    Article  Google Scholar 

  • Picioreanu C, Kreft JU, van Loosdrecht MCM (2004) Particle-based multidimensional multispecies biofilm model. Appl Environ Microbiol 70:3024–3040. doi:10.1128/AEM.70.5.3024-3040.2004

    Article  Google Scholar 

  • Platt TG, Fuqua C (2010) What’s in a name? The semantics of quorum sensing. Trends Microbiol 18:383–387. doi:10.1016/j.tim.2010.05.003

    Article  Google Scholar 

  • Popat R, Crusz SA, Messina M, Williams P, West SA, Diggle SP (2012) Quorum-sensing and cheating in bacterial biofilms. Proc R Soc B 279:4765–4771. doi:10.1098/rspb.2012.1976

    Article  Google Scholar 

  • Pradhan BB, Chatterjee S (2014) Reversible non-genetic phenotypic heterogeneity in bacterial quorum sensing. Mol Microbiol 22:557–569. doi:10.1111/mmi.12575

    Article  Google Scholar 

  • Queller DC (1992) Quantitative genetics, inclusive fitness, and group selection. Am Nat pp 540–558

  • Redfield RJ (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10:365–370. doi:10.1016/S0966-842X(02)02400-9

    Article  Google Scholar 

  • Romero-Campero FJ, Pérez-Jiménez MJ (2008) A model of the quorum sensing system in Vibrio fischeri using p systems. Artif Life 14:95–109. doi:10.1162/artl.2008.14.1.95

    Article  Google Scholar 

  • Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS, West SA (2009) Quorum sensing and the social evolution of bacterial virulence. Curr Biol 19:341–345. doi:10.1016/j.cub.2009.01.050

    Article  Google Scholar 

  • Schaadt N, Steinbach A, Hartmann R, Helms V (2013) Rule-based regulatory and metabolic model for quorum sensing in P. aeruginosa. BMC Syst Biol 7:81. doi:10.1186/1752-0509-7-81

    Article  Google Scholar 

  • Sepulchre JA, Reverchon S, Nasser W (2007) Modeling the onset of virulence in a pectinolytic bacterium. J Theor Biol 244:239–257. doi:10.1016/j.jtbi.2006.08.010

    Article  MathSciNet  Google Scholar 

  • Smith R, Coast J (2013) The true cost of antimicrobial resistance. BMJ 346. doi:10.1136/bmj.f1493

  • Stacy AR, Diggle SP, Whiteley M (2012) Rules of engagement: defining bacterial communication. Curr Opin Microbiol 15:155–161. doi:10.1016/j.mib.2011.11.007

    Article  Google Scholar 

  • Taga ME, Bassler BL (2003) Chemical communication among bacteria. Proc Natl Acad Sci USA 100:14549–14554. doi:10.1073/pnas.1934514100

    Article  Google Scholar 

  • Tang W, Wu Q, Saunders J (2006) A novel model for bacterial foraging in varying environments. In: Gavrilova M, Gervasi O, Kumar V, Tan C, Taniar D, Laganá A, Mun Y, Choo H (eds) Computational science and its applications-ICCSA 2006, vol. 3980 of Lecture Notes in Computer Science, Springer, Berlin, pp 556–565

  • Tang W, Wu Q, Saunders J (2007) Individual-based modeling of bacterial foraging with quorum sensing in a time-varying environment. In: Marchiori E, Moore J, Rajapakse J (eds) Evolutionary computation,machine learning and data mining in bioinformatics, vol. 4447 of Lecture Notes in Computer Science, Springer, Berlin, pp 280–290. doi:10.1007/978-3-540-71783-6_27

  • Tanouchi Y, Tu D, Kim J, You L (2008) Noise reduction by diffusional dissipation in a minimal quorum sensing motif. PLoS Comput Biol 4:e1000167. doi:10.1371/journal.pcbi.1000167

    Article  Google Scholar 

  • Teng SW, Wang Y, Tu KC, Long T, Mehta P, Wingreen NS, Bassler BL, Ong N (2010) Measurement of the copy number of the master quorum-sensing regulator of a bacterial cell. Biophys J 98:2024–2031. doi:10.1016/j.bpj.2010.01.031

    Article  Google Scholar 

  • Tu KC, Long T, Svenningsen SL, Wingreen NS, Bassler BL (2010) Negative feedback loops involving small regulatory RNAs precisely control the vibrio harveyi quorum-sensing response. Mol Cell 37:567–579. doi:10.1016/j.molcel.2010.01.022

    Article  Google Scholar 

  • Uecker H, Müller J, Hense B (2014) Individual-based model for quorum sensing with background flow. Bull Math Biol 76:1727–1746. doi:10.1007/s11538-014-9974-2

    Article  MathSciNet  MATH  Google Scholar 

  • Ullner E, Zaikin A, Volkov EI, García-Ojalvo J (2007) Multistability and clustering in a population of synthetic genetic oscillators via phase-repulsive cell-to-cell communication. Phys Rev Lett 99:148103. doi:10.1103/PhysRevLett.99.148103

    Article  Google Scholar 

  • Uroz S, Chhabra SR, Cámara M, Williams P, Oger P, Dessaux Y (2005) N-acylhomoserine lactone quorum-sensing molecules are modified and degraded by rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151(10):3313–3322. doi:10.1099/mic.0.27961-0

    Article  Google Scholar 

  • Vainstein V, Kirnasovsky OU, Kogan Y, Agur Z (2012) Strategies for cancer stem cell elimination: Insights from mathematical modeling. J Theor Biol 298:32–41. doi:10.1016/j.jtbi.2011.12.016

    Article  MathSciNet  Google Scholar 

  • van Gestel J, Nowak MA, Tarnita CE (2012) The evolution of cell-to-cell communication in a sporulating bacterium. PLoS Comput Biol 8:e1002818. doi:10.1371/journal.pcbi.1002818

    Article  MathSciNet  Google Scholar 

  • Vaughan B, Smith B, Chopp DL (2010) The influence of fluid flow on modeling quorum sensing in bacterial biofilms. Bull Math Biol 72(5):1143–1165. doi:10.1007/s11538-009-9485-8

    Article  MATH  Google Scholar 

  • Viretta AU, Fussenegger M (2004) Modeling the quorum sensing regulatory network of human-pathogenic Pseudomonas aeruginosa. Biotechnol Prog 20:670–678. doi:10.1021/bp034323l

    Article  Google Scholar 

  • Wang M, Schaefer AL, Dandekar AA, Greenberg EP (2015) Quorum sensing and policing of Pseudomonas aeruginosa social cheaters. Proc Natl Acad Sci USA 112:2187–2191. doi:10.1073/pnas.1500704112

    Article  Google Scholar 

  • Ward J (2008) Mathematical modeling of quorum-sensing control in biofilms. In: Balaban N (ed) Control of biofilm infections by signal manipulation, vol. 2 of Springer Series on Biofilms. Springer, Berlin, pp 79–108

  • Ward J, King J (2012) Thin-film modelling of biofilm growth and quorum sensing. J Eng Math 73:71–92. doi:10.1007/s10665-011-9490-4

    Article  MathSciNet  Google Scholar 

  • Ward JP, King JR, Koerber AJ, Croft JM, Sockett RE, Williams P (2003) Early development and quorum sensing in bacterial biofilms. J Math Biol 47:23–55. doi:10.1007/s00285-002-0190-6

    Article  MathSciNet  MATH  Google Scholar 

  • Ward JP, King JR, Koerber AJ, Croft JM, Sockett RE, Williams P (2004) Cell-signalling repression in bacterial quorum sensing. Math Med Biol 21:169–204. doi:10.1093/imammb/21.3.169

    Article  MATH  Google Scholar 

  • Ward JP, King JR, Koerber AJ, Williams P, Croft JM, Sockett RE (2001) Mathematical modelling of quorum sensing in bacteria. Math Med Biol 18:263–292. doi:10.1093/imammb/18.3.263

    Article  MATH  Google Scholar 

  • 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

    Article  Google Scholar 

  • Weber M, 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

    Article  Google Scholar 

  • West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Biol 17:R661–R672

    Article  Google Scholar 

  • West SA, Winzer K, Gardner A, Diggle S (2012) Quorum sensing and the confusion about diffusion. Trends Microbiol 20:586–594. doi:10.1016/j.tim.2012.09.004

    Article  Google Scholar 

  • Whitaker RD, Pember S, Wallace BC, Brodley CE, Walt DR (2011) Single cell time-resolved quorum responses reveal dependence on cell density and configuration. J Biol Chem 286:21623–21632. URL: http://www.jbc.org/content/286/24/21623.abstract

  • Wilder CN, Allada G, Schuster M (2009) Instantaneous within-patient diversity of Pseudomonas aeruginosa quorum-sensing populations from cystic fibrosis lung infections. Infect Immun 77:5631–5639

    Article  Google Scholar 

  • Williams JW, Cui X, Levchenko A, Stevens AM (2008) Robust and sensitive control of a quorum-sensing circuit by two interlocked feedback loops. Mol Syst Biol 4:234–234. doi:10.1038/msb.2008.70

    Article  Google Scholar 

  • Winzer K, Hardie KR, Williams P (2002) Bacterial cell-to-cell communication: sorry, can’t talk now gone to lunch!. Curr Opin Microbiol 5:216–222. doi:10.1016/S1369-5274(02)00304-1

    Article  Google Scholar 

  • Wynendaele E, Bronselaer A, Nielandt J, D’Hondt M, Stalmans S, Bracke N, Verbeke F, Van De Wiele C, De Tré G, De Spiegeleer B (2013) Quorumpeps database: chemical space, microbial origin and functionality of quorum sensing peptides. Nucleic Acids Res 41:655–659. doi:10.1093/nar/gks1137

    Article  Google Scholar 

  • You L, Cox RS, Weiss R, Arnold FH (2004) Programmed population control by cell-cell communication and regulated killing. Nature 428:868–871. doi:10.1038/nature02491

    Article  Google Scholar 

  • Zhou T, Zhang J, Yuan Z, Chen L (2008) Synchronization of genetic oscillators. Chaos 18. doi:10.1063/1.2978183

  • Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci 99:3129–3134

    Article  Google Scholar 

Download references

Acknowledgments

RGC was supported by a grant from SEP/CONACyT-Mexico No. 152794. JPV wants to thank Stephen Starck (TUM) for his patience and help revising the document.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Judith Pérez-Velázquez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez-Velázquez, J., Gölgeli, M. & García-Contreras, R. Mathematical Modelling of Bacterial Quorum Sensing: A Review. Bull Math Biol 78, 1585–1639 (2016). https://doi.org/10.1007/s11538-016-0160-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11538-016-0160-6

Keywords

Mathematics Subject Classification

Navigation