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Quorum sensing for population-level control of bacteria and potential therapeutic applications

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Abstract

Quorum sensing (QS), a microbial cell-to-cell communication process, dynamically regulates a variety of metabolism and physiological activities. In this review, we provide an update on QS applications based on autoinducer molecules including acyl-homoserine lactones (AHLs), auto-inducing peptides (AIPs), autoinducer 2 (AI-2) and indole in population-level control of bacteria, and highlight the potential in developing novel clinical therapies. We summarize the development in the combination of various genetic circuits such as genetic oscillators, toggle switches and logic gates with AHL-based QS devices in Gram-negative bacteria. An overview is then offered to the state-of-the-art of much less researched applications of AIP-based QS devices with Gram-positive bacteria, followed by a review of the applications of AI-2 and indole based QS for interspecies communication among microbial communities. Building on these general-purpose QS applications, we highlight the disruptions and manipulations of QS devices as potential clinical therapies for diseases caused by biofilm formation, antibiotic resistance and the phage invasion. The last part of reviewed literature is dedicated to mathematical modelling for QS applications. Finally, the key challenges and future perspectives of QS applications in monoclonal synthetic biology and synthetic ecology are discussed.

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Abbreviations

[A]:

Intracellular AHL concentration (mM)

[C]:

Intracellular CI protein concentration (mM)

[E]:

Intracellular CcdB protein concentration (mM)

[L]:

Intracellular LacR concentration (mM)

[LuxR]:

Intracellular LuxR concentration (mM)

[R]:

Intracellular AHL/LuxR complex concentration (mM)

N :

The cell density (CFU ml−1)

N m :

The maximum cell density (CFU ml−1)

F pfk :

The fractional Pfk-1 activity (U/mg)

Kd:

The cumulative dissociation constant

X :

Biomass concentration (g L−1)

n1, n2 :

Transcription factor cooperativity/multimerization

α C :

CI protein synthesis rate constant (μM min−1)

αL1, αL2 :

LacR protein synthesis rate constants (μM min−1)

β C :

CI repression coefficient (mM)

β L :

LacR repression coefficient (mM)

d :

Cell death rate (nM−1 h−1)

dA, dE :

AHL and CcdB protein decay constant (min−1)

d C :

CI protein decay constant (min−1)

dL, dR :

LacR and LuxR–AHL complex decay constants (min−1)

k :

Growth rate (h−1)

k E :

CcdB protein production rate constant (h−1)

v A :

AHL production rate constant (nM mL h−1)

θ R :

LuxR/AHL activation coefficient (mM)

ρ R :

LuxR/AHL dimerization constant (μM−3 min−1)

References

  1. Homer CM, Summers DK, Goranov AI, Clarke SC, Wiesner DL, Diedrich JK, Moresco JJ, Toffaletti D, Upadhya R, Caradonna I, Petnic S, Pessino V, Cuomo CA, Lodge JK, Perfect J, Yates JR 3rd, Nielsen K, Craik CS, Madhani HD (2016) Intracellular action of a secreted peptide required for fungal virulence. Cell Host Microbe 19:849–864

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Erez Z, Steinberger-Levy I, Shamir M, Doron S, Stokar-Avihail A, Peleg Y, Melamed S, Leavitt A, Savidor A, Albeck S (2017) Communication between viruses guides lysis-lysogeny decisions. Nature 541:488–493

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Melissa B, Miller BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55(1):165–199

    Google Scholar 

  4. Whiteley M, Diggle SP, Greenberg EP (2017) Progress in and promise of bacterial quorum sensing research. Nature 551:313–320

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Chubukov V, Gerosa L, Kochanowski K, Sauer U (2014) Coordination of microbial metabolism. Nat Rev Microbiol 12:327–340

    CAS  PubMed  Google Scholar 

  6. Holtz WJ, Keasling JD (2010) Engineering static and dynamic control of synthetic pathways. Cell 140:19–23

    CAS  PubMed  Google Scholar 

  7. Venayak N, Anesiadis N, Cluett WR, Mahadevan R (2015) Engineering metabolism through dynamic control. Curr Opin Biotechnol 34:142–152

    CAS  PubMed  Google Scholar 

  8. Gupta A, Reizman IM, Reisch CR, Prather KL (2017) Dynamic regulation of metabolic flux in engineered bacteria using a pathway-independent quorum-sensing circuit. Nat Biotechnol 35:273–279

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Liu D, Evans T, Zhang F (2015) Applications and advances of metabolite biosensors for metabolic engineering. Metab Eng 31:35–43

    PubMed  Google Scholar 

  10. Soma Y, Hanai T (2015) Self-induced metabolic state switching by a tunable cell density sensor for microbial isopropanol production. Metab Eng 30:7–15

    CAS  PubMed  Google Scholar 

  11. Doong SJ, Gupta A, Prather KLJ (2018) Layered dynamic regulation for improving metabolic pathway productivity in escherichia coli. Proc Natl Acad Sci USA 115(12):2964–2969

    CAS  PubMed  Google Scholar 

  12. Liu X, Li XB, Jiang J, Liu ZN, Qiao B, Li FF, Cheng JS, Sun X, Yuan YJ, Qiao J (2018) Convergent engineering of syntrophic Escherichia coli coculture for efficient production of glycosides. Metab Eng 47:243–253

    CAS  PubMed  Google Scholar 

  13. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403(6767):339–342

    CAS  PubMed  Google Scholar 

  14. Elowitz MB, Leibler S (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403:335–338

    CAS  PubMed  Google Scholar 

  15. Win MN, Smolke CD (2007) A modular and extensible rna-based gene-regulatory platform for engineering cellular function. Proc Natl Acad Sci USA 104:14283–14288

    CAS  PubMed  Google Scholar 

  16. Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KL, Keasling JD (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27(8):753–759

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Papenfort K, Bassler BL (2016) Quorum sensing signal–response systems in gram-negative bacteria. Nat Rev Microbiol 14:576–588

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Diggle SP, Griffin AS, Campbell GS, West SA (2007) Cooperation and conflict in quorum-sensing bacterial populations. Nature 450:411–414

    CAS  PubMed  Google Scholar 

  20. Modi SR, Collins JJ, Relman DA (2014) Antibiotics and the gut microbiota. J Clin Investig 124:4212–4218

    CAS  PubMed  Google Scholar 

  21. Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575

    CAS  PubMed  Google Scholar 

  22. Yan J, Bassler BL (2019) Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host Microbe 26:15–21

    CAS  PubMed  Google Scholar 

  23. Hong SH, Hegde M, Kim J, Wang X, Jayaraman A, Wood TK (2012) Synthetic quorum-sensing circuit to control consortial biofilm formation and dispersal in a microfluidic device. Nat Commun 3:613–620

    PubMed  PubMed Central  Google Scholar 

  24. Cho I, Yamanishi S, Cox L, Methé BA, Zavadil J, Li K, Gao Z, Mahana D, Raju K, Teitler I (2012) Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488:621–626

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245

    CAS  PubMed  Google Scholar 

  26. Ma S, Zhou Z (2017) Recent advances in the discovery of pqsd inhibitors as antimicrobial agents. ChemMedChem 12:420–425

    PubMed  Google Scholar 

  27. Thompson JA, Oliveira RA, Djukovic A, Ubeda C, Xavier KB (2015) Manipulation of the quorum sensing signal ai-2 affects the antibiotic-treated gut microbiota. Cell Rep 10:1861–1871. https://doi.org/10.1016/j.celrep.2015.02.049

    Article  CAS  PubMed  Google Scholar 

  28. Abedon ST (2012) Spatial vulnerability: bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 4:663–687

    PubMed  PubMed Central  Google Scholar 

  29. Semenova E, Severinov K (2016) Come together: Crispr-cas immunity senses the quorum. Mol Cell 64:1013–1015

    CAS  PubMed  Google Scholar 

  30. Hawver LA, Jung SA, Ng WL (2016) Specificity and complexity in bacterial quorum-sensing systems. FEMS Microbiol Rev 40:738–752

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Monnet V, Gardan R (2015) Quorum-sensing regulators in gram-positive bacteria: ‘Cherchez le peptide’. Mol Microbiol 97:181–184

    CAS  PubMed  Google Scholar 

  32. Monnet V, Juillard V, Gardan R (2014) Peptide conversations in gram-positive bacteria. Crit Rev Microbiol 42:339–351

    PubMed  Google Scholar 

  33. Lee JH, Wood TK, Lee J (2015) Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol 23:707–718

    CAS  PubMed  Google Scholar 

  34. Hmelo LR (2017) Quorum sensing in marine microbial environments. Ann Rev Mar Sci 9:257–281

    PubMed  Google Scholar 

  35. Zhou L, Zhang LH, Camara M, He YW (2017) The dsf family of quorum sensing signals: diversity, biosynthesis, and turnover. Trends Microbiol 25:293–303

    CAS  PubMed  Google Scholar 

  36. Xu P (2017) Production of chemicals using dynamic control of metabolic fluxes. Curr Opin Biotechnol 53:12–19

    PubMed  Google Scholar 

  37. Shong J, Diaz MRJ, Collins CH (2012) Towards synthetic microbial consortia for bioprocessing. Curr Opin Biotechnol 23:798–802

    CAS  PubMed  Google Scholar 

  38. Song H, Ding MZ, Jia XQ, Ma Q, Yuan YJ (2014) Synthetic microbial consortia: from systematic analysis to construction and applications. Chem Soc Rev 43:6954–6981

    CAS  PubMed  Google Scholar 

  39. Dolinsek J, Goldschmidt F, Johnson DR (2016) Synthetic microbial ecology and the dynamic interplay between microbial genotypes. FEMS Microbiol Rev 40:961–979

    CAS  PubMed  Google Scholar 

  40. Asfahl KL, Schuster M, Gibbs K (2017) Social interactions in bacterial cell–cell signaling. FEMS Microbiol Rev 41:92–107

    CAS  PubMed  Google Scholar 

  41. Choudhary S, Schmidt-Dannert C (2010) Applications of quorum sensing in biotechnology. Appl Microbiol Biotechnol 86:1267–1279

    CAS  PubMed  Google Scholar 

  42. Koo H, Allan RN, Howlin RP, Stoodley P, Hall-Stoodley L (2017) Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol 15:740–755

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Mukherjee S, Bassler BL (2019) Bacterial quorum sensing in complex and dynamically changing environments. Nat Rev Microbiol 17:371–382

    CAS  PubMed  Google Scholar 

  44. Goryachev AB (2011) Understanding bacterial cell–cell communication with computational modeling. Chem Rev 111:238–250

    CAS  PubMed  Google Scholar 

  45. Hense BA, Schuster M (2015) Core principles of bacterial autoinducer systems. Microbiol Mol Biol Rev 79:153–169

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Pérez-Velázquez J, Gölgeli M, García-Contreras R (2016) Mathematical modelling of bacterial quorum sensing: a review. Bull Math Biol 78:1–55

    Google Scholar 

  47. Boyer M, Wisniewski-Dye F (2009) Cell–cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 70:1–19

    CAS  PubMed  Google Scholar 

  48. An JH, Goo E, Kim H, Seo YS, Hwang I (2014) Bacterial quorum sensing and metabolic slowing in a cooperative population. Proc Natl Acad Sci USA 111:14912–14917

    CAS  PubMed  Google Scholar 

  49. Goo E, Majerczyk CD, An JH, Chandler JR, Seo YS, Ham H, Lim JY, Kim H, Lee B, Jang MS, Greenberg EP, Hwang I (2012) Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress. Proc Natl Acad Sci USA 109:19775–19780

    CAS  PubMed  Google Scholar 

  50. You L, Cox RS 3rd, Weiss R, Arnold FH (2004) Programmed population control by cell–cell communication and regulated killing. Nature 428:868–871

    CAS  PubMed  Google Scholar 

  51. Balagadde FK, Song H, Ozaki J, Collins CH, Barnet M, Arnold FH, Quake SR, You L (2008) A synthetic escherichia coli predator–prey ecosystem. Mol Syst Biol 4:187–194

    PubMed  PubMed Central  Google Scholar 

  52. Wu F, Lopatkin AJ, Needs DA, Lee CT, Mukherjee S, You L (2019) A unifying framework for interpreting and predicting mutualistic systems. Nat Commun 10:242–251

    PubMed  PubMed Central  Google Scholar 

  53. Din MO, Danino T, Prindle A, Skalak M, Selimkhanov J, Allen K, Julio E, Atolia E, Tsimring LS, Bhatia SN (2016) Synchronized cycles of bacterial lysis for in vivo delivery. Nature 536:81–85

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Mays ZJ, Nair NU (2018) Synthetic biology in probiotic lactic acid bacteria: at the frontier of living therapeutics. Curr Opin Biotechnol 53:224–231

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Scott SR, Din MO, Bittihn P, Xiong L, Tsimring LS, Hasty J (2017) A stabilized microbial ecosystem of self-limiting bacteria using synthetic quorum-regulated lysis. Nat Microbiol 2:17083–17091

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Woods ML, Leon M, Perezcarrasco R, Barnes CP (2016) A statistical approach reveals designs for the most robust stochastic gene oscillators. ACS Synth Biol 5:459–470

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Jörg DJ, Morelli LG, Jülicher F (2018) Chemical event chain model of coupled genetic oscillators. Phys Rev E 97(3–1):1–11 (032409)

    Google Scholar 

  58. Potvin-Trottier L, Lord ND, Vinnicombe G, Paulsson J (2016) Synchronous long-term oscillations in a synthetic gene circuit. Nature 538:514–517

    PubMed  PubMed Central  Google Scholar 

  59. Tu BP, Mcknight SL (2006) Metabolic cycles as an underlying basis of biological oscillations. Nat Rev Mol Cell Biol 7:696–701

    CAS  PubMed  Google Scholar 

  60. Mondragon-Palomino O, Danino T, Selimkhanov J, Tsimring L, Hasty J (2011) Entrainment of a population of synthetic genetic oscillators. Science 333:1315–1319

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Purcell O, Savery NJ, Grierson CS, Bernardo MD (2010) A comparative analysis of synthetic genetic oscillators. J R Soc Interface 7(52):1503–1524

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Barkai N, Leibler S (2000) Circadian clocks limited by noise. Nature 403(6767):267–268

    CAS  PubMed  Google Scholar 

  63. Hasty J, Dolnik M, Rottschäfer V, Collins JJ (2002) Synthetic gene network for entraining and amplifying cellular oscillations. Phys Rev Lett 88(14):1–4 (148101)

    Google Scholar 

  64. Stricker J, Cookson S, Bennett MR, Mather WH, Tsimring LS, Hasty J (2008) A fast, robust and tunable synthetic gene oscillator. Nature 456:516–519

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Kellogg R, Tay S (2015) Noise facilitates transcriptional control under dynamic inputs. Cell 160:381–392

    CAS  PubMed  Google Scholar 

  66. Tokuda IT, Okamoto A, Matsumura R, Takumi T, Akashi M (2017) Potential contribution of tandem circadian enhancers to nonlinear oscillations in clock gene expression. Mol Biol Cell 28(17):2333–2342

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Wintermute EH, Silver PA (2010) Dynamics in the mixed microbial concourse. Genes Dev 24:2603–2614

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Xavier JB (2011) Social interaction in synthetic and natural microbial communities. Mol Syst Biol 7:483–493

    PubMed  PubMed Central  Google Scholar 

  69. Chuang JS (2012) Engineering multicellular traits in synthetic microbial populations. Curr Opin Chem Biol 16:370–378

    CAS  PubMed  Google Scholar 

  70. Scott SR, Hasty J (2016) Quorum sensing communication modules for microbial consortia. ACS Synth Biol 5:969–977

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Mcmillen D, Kopell N, Hasty J, Collins JJ (2002) Synchronizing genetic relaxation oscillators by intercell signaling. Proc Natl Acad Sci USA 99:679–684

    CAS  PubMed  Google Scholar 

  72. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    CAS  PubMed  Google Scholar 

  73. Slager J, Kjos M, Attaiech L, Veening JW (2014) Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell 157:395–406

    CAS  PubMed  Google Scholar 

  74. Baumgart L, Mather W, Hasty J (2017) Synchronized DNA cycling across a bacterial population. Nat Genet 49(8):1282–1285

    CAS  PubMed  Google Scholar 

  75. Prindle A, Samayoa P, Razinkov I, Danino T, Tsimring LS, Hasty J (2012) A sensing array of radically coupled genetic/’biopixels/’. Nature 481:39–44

    CAS  Google Scholar 

  76. Prindle A, Selimkhanov J, Li H, Razinkov I, Tsimring LS, Hasty J (2014) Rapid and tunable post-translational coupling of genetic circuits. Nature 508:387–391

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Levchenko I, Seidel M, Sauer RT, Baker TA (2000) A specificity-enhancing factor for the clpxp degradation machine. Science 289:2354–2356

    CAS  PubMed  Google Scholar 

  78. Chen Y, Kim JK, Hirning AJ, Josić K, Bennett MR (2015) Emergent genetic oscillations in a synthetic microbial consortium. Science 349(6251):986–989

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Feist AM, Palsson BO (2010) The biomass objective function. Curr Opin Microbiol 13:344–349

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Soma Y, Tsuruno K, Wada M, Yokota A, Hanai T (2014) Metabolic flux redirection from a central metabolic pathway toward a synthetic pathway using a metabolic toggle switch. Metab Eng 23:175–184

    CAS  PubMed  Google Scholar 

  81. Kobayashi H, Kaern M, Araki M, Chung K, Gardner TS, Cantor CR, Collins JJ (2004) Programmable cells: interfacing natural and engineered gene networks. Proc Natl Acad Sci USA 101:8414–8419

    CAS  PubMed  Google Scholar 

  82. Anesiadis N, Cluett WR, Mahadevan R (2008) Dynamic metabolic engineering for increasing bioprocess productivity. Metab Eng 10:255–266

    CAS  PubMed  Google Scholar 

  83. Anesiadis N, Kobayashi H, Cluett WR, Mahadevan R (2013) Analysis and design of a genetic circuit for dynamic metabolic engineering. ACS Synth Biol 2:442–452

    CAS  PubMed  Google Scholar 

  84. Honjo H, Iwasaki K, Soma Y, Tsuruno K, Hamada H, Hanai T (2019) Synthetic microbial consortium with specific roles designated by genetic circuits for cooperative chemical production. Metab Eng 55:268–275

    CAS  PubMed  Google Scholar 

  85. Wang EX, Liu Y, Ma Q, Dong XT, Ding MZ, Yuan YJ (2019) Synthetic cell–cell communication in a three-species consortium for one-step vitamin c fermentation. Biotechnol Lett 41:951–961

    CAS  PubMed  Google Scholar 

  86. Tsoi R, Dai Z, You L (2019) Emerging strategies for engineering microbial communities. Biotechnol Adv 37(6):1–9 (107372)

    Google Scholar 

  87. Nandagopal N, Elowitz MB (2011) Synthetic biology: integrated gene circuits. Science 333:1244–1248

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Benenson Y (2012) Biomolecular computing systems: principles, progress and potential. Nat Rev Genet 13(7):455–468

    CAS  PubMed  Google Scholar 

  89. Moon TS, Lou C, Tamsir A, Stanton BC, Voigt CA (2012) Genetic programs constructed from layered logic gates in single cells. Nature 491:249–253

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Baig H, Madsen J (2017) Simulation approach for timing analysis of genetic logic circuits. ACS Synth Biol 6(7):1169–1179

    CAS  PubMed  Google Scholar 

  91. Nielsen AA, Der BS, Shin J, Vaidyanathan P, Paralanov V, Strychalski EA, Ross D, Densmore D, Voigt CA (2016) Genetic circuit design automation. Science 352(aac7341):1–11

    Google Scholar 

  92. Hasty J, McMillen D, Collins JJ (2002) Engineered gene circuits. Nature 420:224–230

    CAS  PubMed  Google Scholar 

  93. Li Z, Rosenbaum MA, Venkataraman A, Tam TK, Katz E, Angenent LT (2011) Bacteria-based and logic gate: a decision-making and self-powered biosensor. Chem Commun 47:3060–3062

    CAS  Google Scholar 

  94. Arugula MA, Shroff N, Katz E, He Z (2012) Molecular and logic gate based on bacterial anaerobic respiration. Chem Commun 48:10174–10176

    CAS  Google Scholar 

  95. Tamsir A, Tabor JJ, Voigt CA (2010) Robust multicellular computing using genetically encoded nor gates and chemical /`wires/’. Nature 469:212–215

    PubMed  PubMed Central  Google Scholar 

  96. Yokobayashi Y, Weiss R, Arnold F (2002) Directed evolution of a genetic circuit. Proc Natl Acad Sci USA 99:16587–16591

    CAS  PubMed  Google Scholar 

  97. Miyamoto T, Razavi S, Derose R, Inoue T (2013) Synthesizing biomolecule-based boolean logic gates. ACS Synth Biol 2:72–82

    CAS  PubMed  Google Scholar 

  98. Shong J, Collins CH (2014) Quorum sensing-modulated and-gate promoters control gene expression in response to a combination of endogenous and exogenous signals. ACS Synth Biol 3:238–246

    CAS  PubMed  Google Scholar 

  99. Hu Y, Yang Y, Katz E, Song H (2015) Programming the quorum sensing-based and gate in shewanella oneidensis for logic gated-microbial fuel cells. Chem Commun 51:4184–4187

    CAS  Google Scholar 

  100. He X, Chen Y, Liang Q, Qi Q (2017) An autoinduced and-gate controlling metabolic pathway dynamically in response to microbial communities and cell physiological state. ACS Synth Biol 6:463–470

    CAS  PubMed  Google Scholar 

  101. Takayanagi Y, Tanaka K, Takahashi H (1994) Structure of the 5′ upstream region and the regulation of the rpos gene of Escherichia coli. Mol Genet Genomics 243:525–531

    CAS  Google Scholar 

  102. Keller L, Surette MG (2006) Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4:249–258

    CAS  PubMed  Google Scholar 

  103. Papadimitriou K, Alegria A, Bron PA, de Angelis M, Gobbetti M, Kleerebezem M, Lemos JA, Linares DM, Ross P, Stanton C, Turroni F, van Sinderen D, Varmanen P, Ventura M, Zuniga M, Tsakalidou E, Kok J (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80:837–890

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Cook LC, Federle MJ (2014) Peptide pheromone signaling in streptococcus and enterococcus. FEMS Microbiol Rev 38:473–492

    CAS  PubMed  Google Scholar 

  105. Marchand N, Collins CH (2016) Synthetic quorum sensing and cell–cell communication in gram-positive bacillus megaterium. ACS Synth Biol 5:597–606

    CAS  PubMed  Google Scholar 

  106. Cooksley CM, Davis IJ, Winzer K, Chan WC, Peck MW, Minton PN (2010) Regulation of neurotoxin production and sporulation by a putative agrbd signaling system in proteolytic clostridium botulinum. Appl Environ Microbiol 76:4448–4460

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Steiner E, Scott J, Minton NP, Winzer K (2012) An agr quorum sensing system that regulates granulose formation and sporulation in clostridium acetobutylicum. Appl Environ Microbiol 78:1113–1122

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Vivant AL, Garmyn D, Gal L, Piveteau P (2014) The agr communication system provides a benefit to the populations of listeria monocytogenes in soil. Front Cell Infect Microbiol 4(160):1–7

    Google Scholar 

  109. Ma M, Li J, Mcclane BA (2015) Structure-function analysis of peptide signaling in the clostridium perfringens agr-like quorum sensing system. J Bacteriol 197:1807–1818

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Yang T, Talgan Y, Paharik AE, Horswill AR, Blackwell HE (2016) Structure-function analyses of a staphylococcus epidermidis autoinducing peptide reveals motifs critical for agrc-type receptor modulation. ACS Chem Biol 11:1982–1991

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Yu Q, Lepp D, Mehdizadeh GI, Wu T, Zhou H, Yin X, Yu H, Prescott JF, Nie SP, Xie MY (2017) The agr-like quorum sensing system is required for necrotic enteritis pathogenesis in poultry caused by clostridium perfringens. Infect Immun 85:e00975-16

    PubMed  PubMed Central  Google Scholar 

  112. Fontaine L, Boutry C, Guédon E, Guillot A, Ibrahim M, Grossiord B, Hols P (2007) Quorum-sensing regulation of the production of blp bacteriocins in Streptococcus thermophilus. J Bacteriol 189:7195–7205

    CAS  PubMed  PubMed Central  Google Scholar 

  113. Håvarstein LS (2010) Increasing competence in the genus streptococcus. Mol Microbiol 78:541–544

    PubMed  Google Scholar 

  114. Mirouze N, Bergé MA, Soulet AL, Mortierbarrière I, Quentin Y, Fichant G, Granadel C, Noirotgros MF, Noirot P, Polard P (2013) Direct involvement of dpra, the transformation-dedicated reca loader, in the shut-off of pneumococcal competence. Proc Natl Acad Sci USA 110:352–361

    Google Scholar 

  115. Reck M, Tomasch J, Wagner-Dobler I (2015) The alternative sigma factor sigx controls bacteriocin synthesis and competence, the two quorum sensing regulated traits in streptococcus mutans. PLoS Genet 11:e1005353

    PubMed  PubMed Central  Google Scholar 

  116. Moreno-GãmS Sorg RA, Domenech A, Kjos M, Weissing FJ, van Doorn GS, Veening JW (2017) Quorum sensing integrates environmental cues, cell density and cell history to control bacterial competence. Nat Commun 8:854–865

    Google Scholar 

  117. Gallego del Sol F, Marina A (2013) Structural basis of rap phosphatase inhibition by phr peptides. PLoS Biol 11:e1001511

    PubMed  PubMed Central  Google Scholar 

  118. Perchat S, Dubois T, Zouhir S, Gominet M, Poncet S, Lemy C, Aumont-Nicaise M, Deutscher J, Gohar M, Nessler S (2011) A cell–cell communication system regulates protease production during sporulation in bacteria of the bacillus cereus group. Mol Microbiol 82:619–633

    CAS  PubMed  Google Scholar 

  119. Zouhir S, Perchat S, Nicaise M, Perez J, Guimaraes B, Lereclus D, Nessler S (2013) Peptide-binding dependent conformational changes regulate the transcriptional activity of the quorum-sensor nprr. Nucleic Acids Res 41:7920–7933

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Grenha R, Slamti L, Nicaise M, Refes Y, Lereclus D, Nessler S (2013) Structural basis for the activation mechanism of the plcr virulence regulator by the quorum-sensing signal peptide papr. Proc Natl Acad Sci USA 110:1047–1052

    CAS  PubMed  Google Scholar 

  121. Slamti L, Perchat S, Huillet E, Lereclus D (2014) Quorum sensing in bacillus thuringiensis is required for completion of a full infectious cycle in the insect. Toxins 6:2239–2255

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Chen Y, Bandyopadhyay A, Kozlowicz BK, Haemig HAH, Tai A, Hu WS, Dunny GM (2017) Mechanisms of peptide sex pheromone regulation of conjugation in enterococcus faecalis. Microbiologyopen 6(e492):1–13

    Google Scholar 

  123. Mashburn-Warren L, Morrison DA, Federle MJ (2010) A novel double-tryptophan peptide pheromone controls competence in streptococcus spp. via an rgg regulator. Mol Microbiol 78:589–606

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Fleuchot B, Guillot A, Mézange C, Besset C, Chambellon E, Monnet V, Gardan R (2013) Rgg-associated shp signaling peptides mediate cross-talk in streptococci. PLoS One 8:e66042

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Parashar V, Aggarwal C, Federle MJ, Neiditch MB (2015) Rgg protein structure-function and inhibition by cyclic peptide compounds. Proc Natl Acad Sci USA 112:5177–5182

    CAS  PubMed  Google Scholar 

  126. Haustenne L, Bastin G, Hols P, Fontaine L (2015) Modeling of the comrs signaling pathway reveals the limiting factors controlling competence in Streptococcus thermophilus. Front Microbiol 6(1413):1–20

    Google Scholar 

  127. Talagas A, Fontaine L, Ledesma-García L, Mignolet J, Li de la Sierra-Gallay I, Lazar N, Aumont-Nicaise M, Federle MJ, Prehna G, Hols P, Nessler S (2016) Structural insights into streptococcal competence regulation by the cell-to-cell communication system comrs. PLoS Pathog 12:e1005980

    PubMed  PubMed Central  Google Scholar 

  128. Underhill SAM, Shields RC, Kaspar JR, Haider M, Burne RA, Hagen SJ (2018) Intracellular signaling through the comrs system in streptococcus mutans genetic competence. mSphere 3(5):e00444-18

    PubMed  PubMed Central  Google Scholar 

  129. Garcíacontreras R, Nuñezlópez L, Jassochávez R, Kwan BW, Belmont JA, Rangelvega A, Maeda T, Wood TK (2014) Quorum sensing enhancement of the stress response promotes resistance to quorum quenching and prevents social cheating. ISME J 9(1):115–125

    Google Scholar 

  130. Bassler BL, Wright M, Showalter RE, Silverman MR (1993) Intercellular signalling in vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786

    CAS  PubMed  Google Scholar 

  131. Chen X (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549

    CAS  PubMed  Google Scholar 

  132. Sedlmayer F, Hell D, Muller M, Auslander D, Fussenegger M (2018) Designer cells programming quorum-sensing interference with microbes. Nat Commun 9(1822):1–13

    CAS  Google Scholar 

  133. Lee JH, Lee J (2010) Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 34:426–444

    CAS  PubMed  Google Scholar 

  134. Wang D, Ding X, Rather PN (2001) Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183:4210–4216

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Bassler BL, Losick R (2006) Bacterially speaking. Cell 125:237–246

    CAS  PubMed  Google Scholar 

  136. De Keersmaecker SC, Sonck K, Vanderleyden J (2006) Let luxs speak up in ai-2 signaling. Trends Microbiol 14:114–119

    PubMed  Google Scholar 

  137. Pereira CS, Thompson JA, Xavier KB (2013) Ai-2-mediated signalling in bacteria. FEMS Microbiol Rev 37:156–181

    CAS  PubMed  Google Scholar 

  138. Xavier KB, Bassler BL (2005) Regulation of uptake and processing of the quorum-sensing autoinducer ai-2 in Escherichia coli. J Bacteriol 187:238–248

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Xavier KB, Bassler BL (2005) Interference with ai-2-mediated bacterial cell–cell communication. Nature 437:750–753

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Armbruster CE, Hong W, Pang B, Weimer KED, Juneau RA, Turner J, Swords WE (2010) Indirect pathogenicity of haemophilus influenzae and moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. Mbio 1:119–121

    Google Scholar 

  141. Newton WA, Snell EE (1965) Formation and interrelationships of tryptophanase and tryptophan synthetases in Escherichia coli. J Bacteriol 89:355–364

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Lee J, Jayaraman A, Wood TK (2007) Indole is an inter-species biofilm signal mediated by sdia. BMC Microbiol 7:1–15

    Google Scholar 

  143. Chant EL, Summers DK (2007) Indole signalling contributes to the stable maintenance of Escherichia coli multicopy plasmids. Mol Microbiol 63:35–43

    CAS  PubMed  Google Scholar 

  144. Lee HH, Molla MN, Cantor CR, Collins JJ (2010) Bacterial charity work leads to population-wide resistance. Nature 467:82–85

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Jintae L, Can A, Cirillo SLG, Cirillo JD, Wood TK (2010) Indole and 7-hydroxyindole diminish Pseudomonas aeruginosa virulence. Microb Biotechnol 2:75–90

    Google Scholar 

  146. Vega NM, Allison KR, Khalil AS, Collins JJ (2011) Signaling-mediated bacterial persister formation. Nat Chem Biol 8:431

    Google Scholar 

  147. Kim YG, Lee JH, Cho MH, Lee J (2011) Indole and 3-indolylacetonitrile inhibit spore maturation in paenibacillus alvei. BMC Microbiol 11:119

    CAS  PubMed  PubMed Central  Google Scholar 

  148. Catalin C, Field CM, Silvia PF, Keyser UF, Summers DK (2012) Indole prevents Escherichia coli cell division by modulating membrane potential. Biochim Biophys Acta Biomembr 1818:1590–1594

    Google Scholar 

  149. Yee DC, Maynard JA, Wood TK (1998) Rhizoremediation of trichloroethylene by a recombinant, root-colonizing pseudomonas fluorescens strain expressing toluene ortho-monooxygenase constitutively. Appl Environ Microbiol 64:112–118

    CAS  PubMed  PubMed Central  Google Scholar 

  150. Han TH, Cho MH, Lee J (2014) Indole oxidation enhances electricity production in an E. coli-catalyzed microbial fuel cell. Biotechnol Bioprocess E 19:126–131

    CAS  Google Scholar 

  151. Lee JH, Kim YG, Kim CJ, Lee JC, Cho MH, Lee J (2012) Indole-3-acetaldehyde from Rhodococcus sp. Bfi 332 inhibits Escherichia coli o157:h7 biofilm formation. Appl Microbiol Biotechnol 96:1071–1078

    CAS  PubMed  Google Scholar 

  152. Lee JH, Cho HS, Kim Y, Kim JA, Banskota S, Cho MH, Lee J (2013) Indole and 7-benzyloxyindole attenuate the virulence of Staphylococcus aureus. Appl Microbiol Biotechnol 97:4543–4552

    CAS  PubMed  Google Scholar 

  153. Lee JH, Kim YG, Baek KH, Cho MH, Lee J (2015) The multifaceted roles of the interspecies signalling molecule indole in Agrobacterium tumefaciens. Environ Microbiol 17:1234–1244

    CAS  PubMed  Google Scholar 

  154. Chu W, Zere TR, Weber MM, Wood TK, Whiteley M, Hidalgo-Romano B Jr, Valenzuela E, Mclean RJ (2012) Indole production promotes Escherichia coli mixed-culture growth with Pseudomonas aeruginosa by inhibiting quorum signaling. Appl Environ Microbiol 78:411–419

    CAS  PubMed  PubMed Central  Google Scholar 

  155. Lee JH, Kim YG, Kim M, Kim E, Choi H, Kim Y, Lee J (2017) Indole-associated predator–prey interactions between the nematode Caenorhabditis elegans and bacteria. Environ Microbiol 19:1776–1790

    CAS  PubMed  Google Scholar 

  156. Tomberlin JK, Crippen TL, Wu G, Griffin AS, Wood TK, Kilner RM (2017) Indole: an evolutionarily conserved influencer of behavior across kingdoms. BioEssays 39(1600203):1–12

    Google Scholar 

  157. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464

    CAS  PubMed  Google Scholar 

  158. Van AH, Van DP, Coenye T (2014) Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol 22:326–333

    Google Scholar 

  159. Lebeaux D, Ghigo JM, Beloin C (2014) Biofilm-related infections: bridging the gap between clinical management and fundamental aspects of recalcitrance toward antibiotics. Microbiol Mol Biol Rev 78:510–543

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Parsek MR, Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33

    CAS  PubMed  Google Scholar 

  161. Deng YY, Wu JE, Tao F, Zhang LH (2011) Listening to a new language: Dsf-based quorum sensing in gram-negative bacteria. Chem Rev 111:160–173

    CAS  PubMed  Google Scholar 

  162. Lebeer S, Claes IJ, Verhoeven TL, Shen C, Lambrichts I, Ceuppens JL, Vanderleyden J, De Keersmaecker SC (2008) Impact of luxs and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus gg. Appl Environ Microbiol 74:4711–4718

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Sun Z, He X, Brancaccio VF, Yuan J, Riedel CU (2014) Bifidobacteria exhibit luxs-dependent autoinducer 2 activity and biofilm formation. PLoS One 9:e88260

    PubMed  PubMed Central  Google Scholar 

  164. Li H, Li X, Wang Z, Fu Y, Ai Q, Dong Y, Yu J (2015) Autoinducer-2 regulates pseudomonas aeruginosa pao1 biofilm formation and virulence production in a dose-dependent manner. BMC Microbiol 15:1–8

    Google Scholar 

  165. Anderson JK, Huang JY, Wreden C, Sweeney EG, Goers J, Remington SJ, Guillemin K (2015) Chemorepulsion from the quorum signal autoinducer-2 promotes Helicobacter pylori biofilm dispersal. mBio 6:e00379

    CAS  PubMed  PubMed Central  Google Scholar 

  166. Xue T, Ni J, Shang F, Chen X, Zhang M (2015) Autoinducer-2 increases biofilm formation via an ica- and bhp-dependent manner in staphylococcus epidermidis rp62a. Microbes Infect 17:345–352

    CAS  PubMed  Google Scholar 

  167. Laganenka L, Colin R, Sourjik V (2016) Corrigendum: chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli. Nat Commun 7:13979

    CAS  PubMed  PubMed Central  Google Scholar 

  168. Papenfort K, Silpe JE, Schramma KR, Cong JP, Seyedsayamdost MR, Bassler BL (2017) A vibrio cholerae autoinducer-receptor pair that controls biofilm formation. Nat Chem Biol 13:551–557

    CAS  PubMed  PubMed Central  Google Scholar 

  169. Liu L, Wu R, Zhang J, Shang N, Li P (2017) D-ribose interferes with quorum sensing to inhibit biofilm formation of Lactobacillus paraplantarum l-zs9. Front Microbiol 8:1860

    PubMed  PubMed Central  Google Scholar 

  170. Ryan RP, Fouhy Y, Garcia BF, Watt SA, Niehaus K, Yang L, Tolker-Nielsen T, Dow JM (2008) Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68:75–86

    CAS  PubMed  Google Scholar 

  171. Dean SN, Chung MC, van Hoek ML (2015) Burkholderia diffusible signal factor signals to Francisella novicida to disperse biofilm and increase siderophore production. Appl Environ Microbiol 81:7057–7066

    CAS  PubMed  PubMed Central  Google Scholar 

  172. An SQ, Tang JL (2018) Diffusible signal factor signaling regulates multiple functions in the opportunistic pathogen Stenotrophomonas maltophilia. BMC Res Notes 11:569–575

    PubMed  PubMed Central  Google Scholar 

  173. Krzyzek P, Gosciniak G (2018) A proposed role for diffusible signal factors in the biofilm formation and morphological transformation of Helicobacter pylori. Turk J Gastroenterol 29:7–13

    PubMed  Google Scholar 

  174. Deng YY, Lim A, Lee J, Chen SH, An SW, Dong YH, Zhang LH (2014) Diffusible signal factor (dsf) quorum sensing signal and structurally related molecules enhance the antimicrobial efficacy of antibiotics against some bacterial pathogens. BMC Microbiol 14:51–59

    PubMed  PubMed Central  Google Scholar 

  175. Barel V, Chalupowicz L, Barash I, Sharabani G, Reuven M, Dror O, Burdman S, Manulis-Sasson S (2015) Virulence and in planta movement of Xanthomonas hortorum pv. Pelargonii are affected by the diffusible signal factor (dsf)-dependent quorum sensing system. Mol Plant Pathol 16:710–723

    CAS  PubMed  PubMed Central  Google Scholar 

  176. Dow JM (2017) Diffusible signal factor-dependent quorum sensing in pathogenic bacteria and its exploitation for disease control. J Appl Microbiol 122:2–11

    CAS  PubMed  Google Scholar 

  177. Allen RC, Popat R, Diggle SP, Brown SP (2014) Targeting virulence: can we make evolution-proof drugs? Nat Rev Microbiol 12:300–308

    CAS  PubMed  Google Scholar 

  178. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an n-acyl homoserine lactonase. Nature 411:813–817

    CAS  PubMed  Google Scholar 

  179. Shen G, Rajan R, Zhu J, Bell CE, Pei D (2006) Design and synthesis of substrate and intermediate analogue inhibitors of s-ribosylhomocysteinase. J Med Chem 49:3003–3011

    CAS  PubMed  Google Scholar 

  180. Zhang M, Jiao X, Hu Y, Sun L (2009) Attenuation of edwardsiella tarda virulence by small peptides that interfere with luxs/autoinducer type 2 quorum sensing. Appl Environ Microbiol 75:3882–3890

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Ni N, Li M, Wang J, Wang B (2009) Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29:65–124

    CAS  PubMed  Google Scholar 

  182. Brackman G, Defoirdt T, Miyamoto C, Bossier P, Calenbergh SV, Nelis H, Coenye T (2008) Cinnamaldehyde and cinnamaldehyde derivatives reduce virulence in vibriospp. By decreasing the DNA-binding activity of the quorum sensing response regulator luxr. BMC Microbiol 8:149

    PubMed  PubMed Central  Google Scholar 

  183. Brackman G, Cos P, Maes L, Nelis HJ, Coenye T (2011) Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother 55:2655–2661

    CAS  PubMed  PubMed Central  Google Scholar 

  184. Christensen QH, Grove TL, Booker SJ, Greenberg EP (2013) A high-throughput screen for quorum-sensing inhibitors that target acyl-homoserine lactone synthases. Proc Natl Acad Sci USA 110:13815–13820

    CAS  PubMed  Google Scholar 

  185. 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

    PubMed  Google Scholar 

  186. Starkey M, Lepine F, Maura D, Bandyopadhaya A, Lesic B, He J, Kitao T, Righi V, Milot S, Tzika A (2014) Identification of anti-virulence compounds that disrupt quorum-sensing regulated acute and persistent pathogenicity. PLoS Pathog 10:e1004321

    PubMed  PubMed Central  Google Scholar 

  187. Ouyang J, Sun F, Feng W, Sun Y, Qiu X, Xiong L, Liu Y, Chen Y (2016) Quercetin is an effective inhibitor of quorum sensing, biofilm formation and virulence factors in Pseudomonas aeruginosa. J Appl Microbiol 120:966–974

    CAS  PubMed  Google Scholar 

  188. Zerfaß C, Chen J, Soyer OS (2018) Engineering microbial communities using thermodynamic principles and electrical interfaces. Curr Opin Biotechnol 50:121–127

    PubMed  Google Scholar 

  189. McCardell RD, Huang S, Green LN, Murray RM (2017) Control of bacterial population density with population feedback and molecular sequestration. https://doi.org/10.1101/225045

    Article  Google Scholar 

  190. Saeidi N, Wong CK, Lo TM, Nguyen HX, Ling H, Leong SS, Poh CL, Chang MW (2011) Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Mol Syst Biol 7(521):1–11

    Google Scholar 

  191. Gupta S, Bram EE, Weiss R (2013) Genetically programmable pathogen sense and destroy. ACS Synth Biol 2:715–723

    CAS  PubMed  Google Scholar 

  192. Hwang IY, Tan MH, Koh E, Ho CL, Poh CL, Chang MW (2014) Reprogramming microbes to be pathogen-seeking killers. ACS Synth Biol 3:228–237

    CAS  PubMed  Google Scholar 

  193. Hwang IY, Koh E, Wong A, March JC, Bentley WE, Lee YS, Chang MW (2017) Engineered probiotic Escherichia coli can eliminate and prevent Pseudomonas aeruginosa gut infection in animal models. Nat Commun 8:15028

    CAS  PubMed  PubMed Central  Google Scholar 

  194. Zhao L, Zhang F, Ding X, Wu G, Lam YY, Wang X, Fu H, Xue X, Lu C, Ma J (2018) Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. Science 359:1151–1156

    CAS  PubMed  Google Scholar 

  195. Wilck N, Matus MG, Kearney SM, Olesen SW, Forslund K, Bartolomaeus H, Haase S, Mähler A, Balogh A, Markó L (2017) Salt-responsive gut commensal modulates th17 axis and disease. Nature 551:585–589

    CAS  PubMed  PubMed Central  Google Scholar 

  196. Crotty MP, Jackson PJ (2017) Terminal room disinfection: how much betr can it get? Lancet 389:765–766

    PubMed  Google Scholar 

  197. Routy B, Le CE, Derosa L, Cpm D, Alou MT, DaillãRe R, Fluckiger A, Messaoudene M, Rauber C, Roberti MP (2018) Gut microbiome influences efficacy of pd-1-based immunotherapy against epithelial tumors. Science 359:91–97

    CAS  PubMed  Google Scholar 

  198. Zou J, Chassaing B, Singh V, Pellizzon M, Ricci M, Fythe MD, Kumar MV, Gewirtz AT (2018) Fiber-mediated nourishment of gut microbiota protects against diet-induced obesity by restoring il-22-mediated colonic health. Cell Host Microbe 23:41–53

    CAS  PubMed  Google Scholar 

  199. Sun Z, Grimm V, Riedel CU (2015) Ai-2 to the rescue against antibiotic-induced intestinal dysbiosis? Trends Microbiol 23:327–328

    CAS  PubMed  Google Scholar 

  200. Kamada N, Kim YG, Sham HP, Vallance BA, Puente JL, Martens EC, Núñez G (2012) Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 336:1325–1329

    CAS  PubMed  PubMed Central  Google Scholar 

  201. Dandekar AA, Greenberg EP (2012) Bacterial quorum sensing and metabolic incentives to cooperate. Science 338:264–266

    CAS  PubMed  PubMed Central  Google Scholar 

  202. Bongaerts GP, Severijnen RS (2016) A reassessment of the propatria study and its implications for probiotic therapy. Nat Biotechnol 34:55–63

    CAS  PubMed  Google Scholar 

  203. Subramanian S, Huq S, Yatsunenko T, Haque R, Mahfuz M, Alam MA, Benezra A, Destefano J, Meier MF, Muegge BD (2014) Persistent gut microbiota immaturity in malnourished bangladeshi children. Nature 510:417–421

    CAS  PubMed  PubMed Central  Google Scholar 

  204. Hsiao A, Ahmed AM, Subramanian S, Griffin NW, Drewry LL Jr, Petri WA, Haque R, Ahmed T, Gordon JI (2014) Members of the human gut microbiota involved in recovery from vibrio cholerae infection. Nature 515:423–426

    CAS  PubMed  PubMed Central  Google Scholar 

  205. Daniel R, Rubens JR, Sarpeshkar R, Lu TK (2013) Synthetic analog computation in living cells. Nature 497:619–623

    CAS  PubMed  Google Scholar 

  206. Bivar Xavier K (2018) Bacterial interspecies quorum sensing in the mammalian gut microbiota. C R Biol 341:297–299

    PubMed  Google Scholar 

  207. Gilmore MS, Lebreton F, Van SW (2013) Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Curr Opin Microbiol 16:10–16

    PubMed  PubMed Central  Google Scholar 

  208. Borrero J, Chen Y, Dunny GM, Kaznessis YN (2015) Modified lactic acid bacteria detect and inhibit multiresistant enterococci. ACS Synth Biol 4:299–306

    CAS  PubMed  Google Scholar 

  209. Arias CA, Murray BE (2012) The rise of the enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 10:266–278

    CAS  PubMed  PubMed Central  Google Scholar 

  210. Coyte KZ, Rakoff-Nahoum S (2019) Understanding competition and cooperation within the mammalian gut microbiome. Curr Biol 29:538–544

    Google Scholar 

  211. Li Q, Ren Y, Fu X (2019) Inter-kingdom signaling between gut microbiota and their host. Cell Mol Life Sci 76:2383–2389

    CAS  PubMed  Google Scholar 

  212. Mirzaei MK, Maurice CF (2017) Menage a trois in the human gut: interactions between host, bacteria and phages. Nat Rev Microbiol 15:397–408

    CAS  PubMed  Google Scholar 

  213. Bondydenomy J, Pawluk A, Maxwell KL, Davidson AR (2013) Bacteriophage genes that inactivate the crispr/cas bacterial immune system. Nature 493:429–432

    CAS  Google Scholar 

  214. Patterson AG, Yevstigneyeva MS, Fineran PC (2017) Regulation of crispr-cas adaptive immune systems. Curr Opin Microbiol 37:1–7

    CAS  PubMed  Google Scholar 

  215. Patterson A, Jackson S, Taylor C, Evans G, Salmond GC, Przybilski R, Staals RJ, Fineran P (2016) Quorum sensing controls adaptive immunity through the regulation of multiple crispr-cas systems. Mol Cell 64:1102–1108

    CAS  PubMed  PubMed Central  Google Scholar 

  216. Brophy JA, Voigt CA (2014) Principles of genetic circuit design. Nat Methods 11:508–520

    CAS  PubMed  PubMed Central  Google Scholar 

  217. Buescher JM (2012) Global network reorganization during dynamic adaptations of bacillus subtilis metabolism. Science 335:1099–1103

    CAS  PubMed  Google Scholar 

  218. Woolston BM, Edgar S, Stephanopoulos G (2013) Metabolic engineering: past and future. Annu Rev Chem Biomol Eng 4:259–288

    CAS  PubMed  Google Scholar 

  219. Orth JD, Thiele I, Palsson BØ (2010) What is flux balance analysis? Nat Biotechnol 28:245–248

    CAS  PubMed  PubMed Central  Google Scholar 

  220. Meadows AL, Karnik R, Lam H, Forestell S, Snedecor B (2010) Application of dynamic flux balance analysis to an industrial escherichia coli fermentation. Metab Eng 12:150–160

    CAS  PubMed  Google Scholar 

  221. Hill A (1913) The combinations of haemoglobin with oxygen and with carbon monoxide. I. Biochem J 7:577–586

    Google Scholar 

  222. Schmidt SK, Simkins S, Alexander M (1985) Models for the kinetics of biodegradation of organic compounds not supporting growth. Appl Environ Microbiol 50:323–331

    CAS  PubMed  PubMed Central  Google Scholar 

  223. English BP, Min W, van Oijen AM, Lee KT, Luo G, Sun H, Cherayil BJ, Kou SC, Xie XS (2006) Ever-fluctuating single enzyme molecules: Michaelis-menten equation revisited. Nat Chem Biol 2:87–94

    CAS  PubMed  Google Scholar 

  224. Basu Subhayu, Gerchman Yoram, Collins Cynthia H, Arnold FH, Weiss R (2005) A synthetic multicellular system for programmed pattern formation. Nature 434:1130–1134

    CAS  PubMed  Google Scholar 

  225. Song H, Stephen P, Meagan G, You L (2009) Spatiotemporal modulation of biodiversity in a synthetic chemical-mediated ecosystem. Nat Chem Biol 5:929–935

    CAS  PubMed  PubMed Central  Google Scholar 

  226. Kong W, Meldgin DR, Collins JJ, Lu T (2018) Designing microbial consortia with defined social interactions. Nat Chem Biol 14:821–829

    CAS  PubMed  Google Scholar 

  227. Mads K, Elston TC, Blake WJ, Collins JJ (2005) Stochasticity in gene expression: from theories to phenotypes. Nat Rev Genet 6:451–464

    Google Scholar 

  228. Tian T, Burrage K (2006) Stochastic models for regulatory networks of the genetic toggle switch. Proc Natl Acad Sci USA 103:8372–8377

    CAS  PubMed  Google Scholar 

  229. Prindle A, Liu J, Asally M, Ly S, Garciaojalvo J, Süel GM (2015) Ion channels enable electrical communication within bacterial communities. Nature 527:59–63

    CAS  PubMed  PubMed Central  Google Scholar 

  230. Popkin G (2017) Bacteria use brainlike bursts of electricity to communicate. Quanta Magazine, New York

    Google Scholar 

  231. Liu J, Zhou J, Wang L, Ma Z, Zhao G, Ge Z, Zhu H, Qiao J (2017) Improving nitrogen source utilization from defatted soybean meal for nisin production by enhancing proteolytic function of Lactococcus lactis f44. Sci Rep 7:6189

    PubMed  PubMed Central  Google Scholar 

  232. Wu H, Song S, Tian K, Zhou D, Wang B, Liu J, Zhu H, Qiao J (2018) A novel small rna s042 increases acid tolerance in Lactococcus lactis f44. Biochem Biophys Res Commun 500:544–549

    CAS  PubMed  Google Scholar 

  233. Song AA, In LLA, Lim SHE, Rahim RA (2017) A review on Lactococcus lactis: from food to factory. Microb Cell Fact 16:55

    PubMed  PubMed Central  Google Scholar 

  234. Guo CJ, Chang FY, Wyche TP, Backus KM, Acker TM, Funabashi M, Mao T, Donia MS, Nayfach S, Pollard KS (2017) Discovery of reactive microbiota-derived metabolites that inhibit host proteases. Cell 168:517–526

    CAS  PubMed  PubMed Central  Google Scholar 

  235. Foster KR, Schluter J, Coyte KZ, Rakoff-Nahoum S (2017) The evolution of the host microbiome as an ecosystem on a leash. Nature 548:43–51

    CAS  PubMed  PubMed Central  Google Scholar 

  236. Fernandez L, Rodriguez A, Garcia P (2018) Phage or foe: an insight into the impact of viral predation on microbial communities. ISME J 12:1171–1179

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by the National Key Research and Development Project of China (2017YFD0201400), the National Natural Science Foundation of China (31570089, 31170076), and the Funds for Creative Research Groups of China (21621004), Dr. Jianjun Qiao was supported by The New Century Outstanding Talent Support Program, Education Ministry of China.

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  1. School of Chemical Engineering and Technology, Tianjin University, Tianjin, 300072, China

    Shengbo Wu, Jiaheng Liu, Chunjiang Liu & Jianjun Qiao

  2. State Key Laboratory of Chemical Engineering, Tianjin University, Tianjin, 300072, China

    Shengbo Wu & Chunjiang Liu

  3. Collaborative Innovation Center of Chemical Science and Engineering (Tianjin), Tianjin, 300072, China

    Shengbo Wu, Jiaheng Liu, Chunjiang Liu & Jianjun Qiao

  4. Key Laboratory of Systems Bioengineering, Ministry of Education (Tianjin University), Tianjin, 300072, China

    Jiaheng Liu & Jianjun Qiao

  5. Department of Engineering Science, University of Oxford, Oxford, OX1 3PJ, UK

    Aidong Yang

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Wu, S., Liu, J., Liu, C. et al. Quorum sensing for population-level control of bacteria and potential therapeutic applications. Cell. Mol. Life Sci. 77, 1319–1343 (2020). https://doi.org/10.1007/s00018-019-03326-8

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