Skip to main content

Advertisement

Log in

Potential Emergence of Multi-quorum Sensing Inhibitor Resistant (MQSIR) Bacteria

  • Review article
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Expression of certain bacterial genes only at a high bacterial cell density is termed as quorum-sensing (QS). Here bacteria use signaling molecules to communicate among themselves. QS mediated genes are generally involved in the expression of phenotypes such as bioluminescence, biofilm formation, competence, nodulation, and virulence. QS systems (QSS) vary from a single in Vibrio spp. to multiple in Pseudomonas and Sinorhizobium species. The complexity of QSS is further enhanced by the multiplicity of signals: (1) peptides, (2) acyl-homoserine lactones, (3) diketopiperazines. To counteract this pathogenic behaviour, a wide range of bioactive molecules acting as QS inhibitors (QSIs) have been elucidated. Unlike antibiotics, QSIs don’t kill bacteria and act at much lower concentration than those of antibiotics. Bacterial ability to evolve resistance against multiple drugs has cautioned researchers to develop QSIs which may not generate undue pressure on bacteria to develop resistance against them. In this paper, we have discussed the implications of the diversity and multiplicity of QSS, in acting as an arsenal to withstand attack from QSIs and may use these as reservoirs to develop multi-QSI resistance.

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.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AI:

Autoinducer

AHL:

Acylhomoserine lactone

HSL:

Homoserine lactone

C4HSL:

N-butanoyl-L-HSL

C6HSL:

N-hexanoyl HSL

C7HSL:

N-heptanoyl-HL

C8HSL:

N-octanoyl HSL

C10HSL:

N-decanoyl HSL

C12HSL:

N-dodecanoyl HSL

C14HSL:

N-tetradecanoyl-HSL

C16HSL:

N-hexadecanoyl-HSL

3OC6HSL:

3-Oxo-N-hexanoyl-HSL

3OC8HSL:

3-Oxo-N-octanoyl-HSL

3OC10HSL:

3-Oxo-N-decanoyl-HSL

3OC12HSL:

3-Oxo-N-dodecanoyl-HSL

3OC14 HSL:

3-Oxo-N-tetradecanoyl-HSL

OHC4HSL:

3-Hydroxy-N-butanoyl-HSL

OHC6HSL:

3-Hydroxy-N-hexanoyl-L-HSL

OHC8HSL:

3-Hydroxy-N-octanoyl-L-HSL

OHC10HSL:

3-Hydroxy-N-decanoyl-HSL

OHC14HSL:

3-Hydroxy-N-tetradecanoyl-HSL

References

  1. Kalia VC (2015) Microbes: the most friendly beings? In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 1–5. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_1

  2. Defoirdt T, Boon N, Bossier P (2010) Can bacteria evolve resistance to quorum sensing disruption? PLoS Pathog 6:e1000989. doi:10.1371/journal.ppat.1000989

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  3. Schuster M, Sexton DJ, Diggle SP, Greenberg EP (2013) Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol 67:43–63. doi:10.1146/annurev-micro-092412-155635

    Article  PubMed  CAS  Google Scholar 

  4. Sajid A, Arora G, Singhal A, Kalia VC, Singh Y (2015) Protein phosphatases of pathogenic bacteria: role in physiology and virulence. Annu Rev Microbiol 69:527–547. doi:10.1146/annurev-micro-020415-111342

    Article  PubMed  CAS  Google Scholar 

  5. Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116. doi:10.1126/science.1121357

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  6. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245. doi:10.1016/j.biotechadv.2012.10.00

    Article  PubMed  CAS  Google Scholar 

  7. Dong Y, Wang L, Zhang L (2007) Quorum-quenching microbial infections: mechanisms and implications. Philos Trans R Soc B362:1201–1211. doi:10.1098/rstb.2007.2045

    Article  CAS  Google Scholar 

  8. Jayaraman A, Wood TK (2008) Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu Rev Biomed Eng 10:145–167. doi:10.1146/annurev.bioeng.10.061807.160536

    Article  PubMed  CAS  Google Scholar 

  9. Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2:a012427. doi:10.1101/cshperspect.a012427

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  10. Kimura N (2014) Metagenomic approaches to understanding phylogenetic diversity in quorum sensing. Virulence 5:433–442. doi:10.4161/viru.27850

    Article  PubMed Central  PubMed  Google Scholar 

  11. Kalia VC (2014) In search of versatile organisms for quorum sensing inhibitors: acyl homoserine lactones (AHL)-acylase and AHL-lactonase. FEMS Microbiol Lett 359:143. doi:10.1111/1574-6968.12585

    Article  PubMed  CAS  Google Scholar 

  12. Kalia VC (2014) Microbes, antimicrobials and resistance: the battle goes on. Indian J Microbiol 54:1–2. doi:10.1007/s12088-013-0443-7

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  13. García-Contreras R, Maeda T, Wood TK (2015) Can resistance against quorum-sensing interference be selected? ISME J. doi:10.1038/ismej.2015.84

    PubMed Central  Google Scholar 

  14. Antunes LC, Schaefer AL, Ferreira RB, Qin N, Stevens AM, Ruby EG, Greenberg EP (2007) Transcriptome analysis of the Vibrio fischeri LuxR–LuxI regulon. J Bacteriol 189:8387–8391. doi:10.1128/JB.00736-07

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  15. Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079. doi:10.1128/JB.185.7.2066-2079.2003

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  16. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185:2080–2095. doi:10.1128/JB.185.7.2080-2095.2003

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  17. Manolescu BN (2013) Paraoxonases as protective agents against N-acyl homoserine lactone—producing pathogenic microorganisms. Maedica (Buchar) J Clin Med 8:49–52

    Google Scholar 

  18. Lee JH, Wood TK, Lee J (2015) Roles of indole as an interspecies and interkingdom signaling molecule. Trends Microbiol. doi:10.1016/j.tim.2015.08.001

    Google Scholar 

  19. Oslizlo A, Stefanic P, Dogsa I, Mandic-Mulec I (2014) Private link between signal and response in Bacillus subtilis quorum sensing. Proc Natl Acad Sci USA 111:1586–1591. doi:10.1073/pnas.1316283111

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  20. Ganin H, Yardeni EH, Kolodkin-Gal I (2015) Biofilms: maintenance, development, and disassembly of bacterial communities are determined by QS cascades. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 23–37. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_3

  21. Kalia VC, Mukherjee T, Bhushan A, Joshi J, Shankar P, Huma N (2011) Analysis of the unexplored features of rrs (16S rDNA) of the genus Clostridium. BMC Genom 12:18. doi:10.1186/1471-2164-12-18

    Article  CAS  Google Scholar 

  22. Bhushan A, Mukherjee T, Joshi J, Shankar P, Kalia VC (2015) Insights into the origin of Clostridium botulinum strains: evolution of distinct restriction endonuclease sites in rrs (16S rRNA gene). Indian J Microbiol 55:140–150. doi:10.1007/s12088-015-0514-z

    Article  PubMed  Google Scholar 

  23. Kekre A, Bhushan A, Kumar P, Kalia VC (2015) Genome wide analysis for searching novel markers to rapidly identify Clostridium strains. Indian J Microbiol 55:250–257. doi:10.1007/s12088-015-0535-7

    Article  PubMed  CAS  Google Scholar 

  24. Ohtani K, Bhowmik SK, Hayashi H, Shimizu T (2002) Identification of a novel locus that regulates expression of toxin genes in Clostridium perfringens. FEMS Microbiol Lett 209:113–118. doi:10.1111/j.1574-6968.2002.tb11118.x

    Article  PubMed  CAS  Google Scholar 

  25. Carter GP, Purdy D, Williams P, Minton NP (2005) Quorum sensing in Clostridium difficile: analysis of a luxS-type signalling system. J Med Microbiol 54:119–127. doi:10.1099/jmm.0.45817-0

    Article  PubMed  CAS  Google Scholar 

  26. Cooksley CM, Davis IJ, Winzer K, Chan WC, Peck MW, Minton NP (2010) Regulation of neurotoxin production and sporulation by a putative agrBD signaling system in proteolytic Clostridium botulinum. Appl Environ Microbiol 76:4448–4460. doi:10.1128/AEM.03038-09

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Li J, Chen J, Vidal JE, McClane BA (2011) The Agr-like quorum-sensing system regulates sporulation and production of enterotoxin and beta2 toxin by Clostridium perfringens type A non-food-borne human gastrointestinal disease strain F5603. Infect Immun 79:2451–2459. doi:10.1128/AI.00169-11

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  28. Pinkston KL, Gao P, Diaz-Garcia D, Sillanpää J, Nallapareddy SR, Murray BE, Barrett R, Harvey BR (2011) The Fsr quorum-sensing system of Enterococcus faecalis modulates surface display of the collagen-binding MSCRAMM ace through regulation of gelE. J Bacteriol 193:4317–4325. doi:10.1128/JB.05026-11

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  29. Marketon MM, Gronquist MR, Eberhard A, González JE (2002) Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J Bacteriol 184:5686–5695. doi:10.1128/JB.184.20.5686-5695.2002

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  30. Knutsen E, Ween O, Håvarstein LS (2004) Two separate quorum-sensing systems upregulate transcription of the same ABC transporter in Streptococcus pneumonia. J Bacteriol 186:3078–3085. doi:10.1128/JB.186.10.3078-3085.2004

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  31. Martin MJ, Clare S, Goulding D, Faulds-Pain A, Barquist L, Browne HP, Pettit L, Dougan G, Lawley TD, Wren BW (2013) The agr locus regulates virulence and colonization genes in Clostridium difficile 027. J Bacteriol 195:3672–3681. doi:10.1128/JB.00473-13

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  32. Li YH, Tian X (2012) Quorum sensing and bacterial social interactions in biofilms. Sensors 12:2519–2538. doi:10.3390/s120302519

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  33. Kaur G, Rajesh S, Princy SA (2015) Plausible drug targets in the Streptococcus mutans quorum sensing pathways to combat dental biofilms and associated risks. Indian J Microbiol 55:349–357. doi:10.1007/s12088-015-0534-8

    Article  PubMed  CAS  Google Scholar 

  34. Lyon WR, Madden JC, Levin JC, Stein JL, Caparon MG (2001) Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42:145–157. doi:10.1046/j.1365-2958.2001.02616.x

    Article  PubMed  CAS  Google Scholar 

  35. Rai N, Rai R, Venkatesh KV (2015) Quorum sensing in competence and sporulation. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 61–64. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_6

  36. Gray B, Hall P, Gresham H (2013) Targeting agr- and agr-like quorum sensing systems for development of common therapeutics to treat multiple gram-positive bacterial infections. Sensors 13:5130–5166. doi:10.3390/s130405130

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  37. Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052. doi:10.1371/journal.ppat.1000052

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  38. Lyon GJ, Novick RP (2004) Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25:1389–1403. doi:10.1016/j.peptides.2003.11.026

    Article  PubMed  CAS  Google Scholar 

  39. Riedel CU, Monk IR, Casey PG, Waidmann MS, Gahan CGM, Hill C (2009) AgrD-dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Mol Microbiol 71:1177–1189. doi:10.1111/j.1365-2958.2008.06589.x

    Article  PubMed  CAS  Google Scholar 

  40. Urbanowski ML, Lostroh CP, Greenberg EP (2004) Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J Bacteriol 186:631–637. doi:10.1128/JB.186.3.631-637.2004

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  41. Lupp C, Urbanowski M, Greenberg EP, Ruby EG (2003) The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol Microbiol 50:319–331. doi:10.1046/j.1365-2958.2003.t01-1-03585.x

    Article  PubMed  CAS  Google Scholar 

  42. Lilley BN, Bassler BL (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol Microbiol 60:331–348. doi:10.1046/j.1365-2958.2000.01913.x

    Google Scholar 

  43. Antunes LCM, Ferreira RBR (2009) Intercellular communication in bacteria. Crit Rev Microbiol 35:69–80. doi:10.1080/10408410902733946

    Article  PubMed  CAS  Google Scholar 

  44. Hema M, Balasubramanian S, Princy SA (2015) Meddling Vibrio cholerae murmurs: a neoteric advancement in cholera research. Indian J Microbiol 55:121–130. doi:10.1007/s12088-015-0520-1

    Article  PubMed  CAS  Google Scholar 

  45. Ng WL, Perez L, Cong J, Semmelhack MF, Bassler BL (2012) Broad spectrum pro-quorum-sensing molecules as inhibitors of virulence in vibrios. PLoS Pathog 8:e1002767. doi:10.1371/journal.ppat.1002767

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  46. Hammer BK, Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholera. Mol Microbiol 50:101–104. doi:10.1046/j.1365-2958.2003.03688.x

    Article  PubMed  CAS  Google Scholar 

  47. Lenz DH, Miller MB, Zhu J, Kulkarni RV, Bassler BL (2005) CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol 58:1186–1202. doi:10.1111/j.1365-2958.2005.04902.x

    Article  PubMed  CAS  Google Scholar 

  48. Kelly RC, Bolitho ME, Higgins DA, Lu W, Ng W-L, Jeffrey PD, Rabinowitz JD, Semmelhack MF, Hughson FM, Bassler BL (2009) The Vibrio cholerae quorum-sensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat Chem Biol 5:891–895. doi:10.1038/nchembio.237

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  49. Henke JM, Bassler BL (2004) Bacterial social engagements. Trends Cell Biol 14:648–656. doi:10.1128/JB.186.20.6902

    Article  PubMed  CAS  Google Scholar 

  50. Henke JM, Bassler BL (2004) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186:6902–6914. doi:10.1128/JB.186.20.6902-6914.2004

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  51. Timmen M, Bassler BL, Jung K (2006) AI-1 influences the kinase activity but not the phosphatase activity of LuxN of Vibrio harveyi. J Biol Chem 281:24398–24404. doi:10.1074/jbc.M604108200

    Article  PubMed  CAS  Google Scholar 

  52. Anetzberger C, Reiger M, Fekete A, Schell U, Stambrau N, Plener L, Kopka J, Schmitt-Kopplin P, Hilbi H, Jung K (2012) Autoinducers act as biological timers in Vibrio harveyi. PLoS One 7:e48310. doi:10.1371/journal.pone.0048310

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  53. Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM (2005) Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 18:507–518. doi:10.1016/j.molcel.2005.04.020

    Article  PubMed  CAS  Google Scholar 

  54. Ng WL, Perez LJ, Wei Y, Kraml C, Semmelhack MF, Bassler BL (2011) Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol Microbiol 79:1407–1417. doi:10.1111/j.1365-2958.2011.07548.x

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  55. Wei Y, Ng WL, Cong J, Bassler BL (2012) Ligand and antagonist driven regulation of the Vibrio cholerae quorum-sensing receptor CqsS. Mol Microbiol 83:1095–1108. doi:10.1111/j.1365-2958.2012.07992.x

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  56. Lin W, Kovacikova G, Skorupski K (2007) The quorum sensing regulator HapR downregulates the expression of the virulence gene transcription factor AphA in Vibrio cholerae by antagonizing Lrp- and VpsR-mediated activation. Mol Microbiol 64:953–967. doi:10.1111/j.1365-2958.2007.05693.x

    Article  PubMed  CAS  Google Scholar 

  57. Rutherford ST, van Kessel JC, Shao Y, Bassler BL (2011) AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev 25:397–408. doi:10.1101/gad.2015011

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  58. Withey JH, DiRita VJ (2006) The toxbox: specific DNA sequence requirements for activation of Vibrio cholerae virulence genes by ToxT. Mol Microbiol 59:1779–1789. doi:10.1111/j.1365-2958.2006.05053.x

    Article  PubMed  CAS  Google Scholar 

  59. Matson JS, Withey JH, DiRita VJ (2007) Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun 75:5542–5549. doi:10.1128/IAI.01094-07

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  60. Schuster M, Greenberg EP (2007) Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genom 8:287. doi:10.1186/1471-2164-8-287

    Article  CAS  Google Scholar 

  61. McKnight SL, Iglewski BH, Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 182:2702–2708. doi:10.1128/JB.182.10.2702-2708.2000

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  62. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Cámara M, Williams P (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43. doi:10.1046/j.1365-2958.2003.03672.x

    Article  PubMed  CAS  Google Scholar 

  63. Bredenbruch F, Geffers R, Nimtz M, Buer J, Häussler S (2006) The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 8:1318–1329. doi:10.1111/j.1462-2920.2006.01025.x

    Article  PubMed  CAS  Google Scholar 

  64. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Høiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815. doi:10.1093/emboj/cdg366

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  65. Chugani SA, Whiteley M, Lee KM, D’Argenio D, Manoil C, Greenberg EP (2001) QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 98:2752–2757. doi:10.1073/pnas.051624298

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  66. LequetteY Lee JH, Ledgham F, Lazdunski A, Greenberg EP (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188:3365–3370. doi:10.1128/JB.188.9.3365-3370.200

    Article  CAS  Google Scholar 

  67. De Carvalho MP, Abraham WR (2012) Antimicrobial and biofilm inhibiting diketopiperazines. Curr Med Chem 19:3564–3577. doi:10.2174/092986712801323243

    Article  PubMed  Google Scholar 

  68. Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH, Quax WJ (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46–65. doi:10.1128/MMBR.05007-11

    Article  PubMed  CAS  Google Scholar 

  69. Daniels R, Vanderleyden J, Michiels J (2004) Quorum sensing and swarming migration in bacteria. FEMS Microbiol Rev 28:261–289. doi:10.1016/j.femsre.2003.09.004

    Article  PubMed  CAS  Google Scholar 

  70. Venturi V (2006) Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30:274–291. doi:10.1111/j.1574-6976.2005.00012.x

    Article  PubMed  CAS  Google Scholar 

  71. Khan SR, Herman J, Krank J, Serkova NJ, Churchill ME, Suga H, Farrand SK (2007) N-(3-hydroxyhexanoyl)-L-homoserine lactone is the biologically relevant quormone that regulates the phz operon of Pseudomonas chlororaphis Strain 30–84. Appl Environ Microbiol 73:7443–7455. doi:10.1128/AEM.01354-07

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  72. Laue BE, Jiang Y, Chhabra SR, Jacob S, Stewart GS, Hardman A, Downie JA, O’Gara F, Williams P (2000) The biocontrol strain Pseudomonas fluorescens F113 produces the Rhizobium small bacteriocin, N-(3-hydroxy-7-cis-tetradecenoyl)homoserine lactone, via HdtS, a putative novel N-acylhomoserine lactone synthase. Microbiology 146:2469–2480. doi:10.1099/00221287-146-10-2469

    Article  PubMed  CAS  Google Scholar 

  73. Aswathanarayan JB, Rai VR (2015) Quorum sensing systems in Pseudomonas. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 73–84. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_8

  74. Gao J, Ma A, Zhuang X, Zhuang G (2015) Quorum sensing in nitrogen fixation. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 51–60. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_5

  75. Lithgow JK, Wilkinson A, Hardman A, Rodelas B, Wisniewski-Dyé F, Williams P, Downie JA (2000) The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol Microbiol 37:81–97. doi:10.1046/j.1365-2958.2000.01960.x

    Article  PubMed  CAS  Google Scholar 

  76. Braeken K, Daniels R, Ndayizeye M, Vanderleyden J, Michiels J (2008) Quorum sensing in bacteria-plant interactions. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence, vol 15. Springer, Berlin/Heidelberg, pp 265–289

    Chapter  Google Scholar 

  77. Sanchez-Contreras M, Bauer WD, Gao M, Robinson JB, Allan Downie J (2007) Quorum-sensing regulation in rhizobia and its role in symbiotic interactions with legumes. Philos Trans R Soc B 362:1149–1163. doi:10.1098/rstb.2007.2041

    Article  CAS  Google Scholar 

  78. Frederix M, Edwards A, McAnulla C, Downie JA (2011) Co-ordination of quorum-sensing regulation in Rhizobium leguminosarum by induction of an anti-repressor. Mol Microbiol 81:994–1007. doi:10.1111/j.1365-2958.2011.07738.x

    Article  PubMed  CAS  Google Scholar 

  79. Wilkinson A, Danino V, Wisniewski-Dyé F, Lithgow JK, Downie JA (2002) N-acyl-homoserine lactone inhibition of rhizobial growth is mediated by two quorum-sensing genes that regulate plasmid transfer. J Bacteriol 184:4510–4519. doi:10.1128/JB.184.16.4510-4519.2002

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  80. Wisniewski-Dyé F, Jones J, Chhabra SR, Downie JA (2000) raiIR genes are part of a quorum-sensing network controlled by cinI and cinR in Rhizobium leguminosarum. J Bacteriol 184:1597–1606. doi:10.1128/JB.184.6.1597-1606.2002

    Article  CAS  Google Scholar 

  81. Jones KM, Sharopova N, Lohar DP, Zhang JQ, Vanden-Bosch KA, Walker GC (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci USA 105:704–709. doi:10.1073/pnas.0709338105

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  82. Gao M, Chen H, Eberhard A, Gronquist MR, Robinson JB, Rolfe BG, Bauer WD (2005) sinI- and expR-dependent quorum sensing in Sinorhizobium meliloti. J Bacteriol 187:7931–7944. doi:10.1128/JB.187.23.7931-7944.2005

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  83. Boyer M, Wisniewski-Dye F (2009) Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol Ecol 70:1–19. doi:10.1111/j.1574-6941.2009.00745.x

    Article  PubMed  CAS  Google Scholar 

  84. Glenn SA, Gurich N, Feeney MA, Gonzalez JE (2007) The ExpR/Sin quorum-sensing system controls succinoglycan production in Sinorhizobium meliloti. J Bacteriol 189:7077–7088. doi:10.1128/JB.00906-07

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  85. Rivas M, Seeger M, Jedlicki E, Holmes DS (2007) Second acyl homoserine lactone production system in the extreme acidophile Acidithiobacillus ferrooxidans. Appl Environ Microbiol 73:3225–3231. doi:10.1128/AEM.02948-06

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  86. Wenbin N, Dejuan Z, Feifan L, Lei Y, Peng C, Xiaoxuan Y, Hongyu L (2011) Quorum-sensing system in Acidithiobacillus ferrooxidans involved in its resistance to Cu2+. Lett Appl Microbiol 53:84–89. doi:10.1111/j.1472-765X.2011.03066.x

    Article  PubMed  CAS  Google Scholar 

  87. González A, Bellenberg S, Mamani S, Ruiz L, Echeverría A, Soulère L, Doutheau A, Demergasso C, Sand W, Queneau Y, Vera M, Guiliani N (2013) AHL signaling molecules with a large acyl chain enhance biofilm formation on sulfur and metal sulfides by the bioleaching bacterium Acidithiobacillus ferrooxidans. Appl Microbiol Biotechnol 97:3729–3737. doi:10.1007/s00253-012-4229-3

    Article  PubMed  CAS  Google Scholar 

  88. González Barrios AF, Zuo R, Hashimoto Y, Yang L, Bentley WE, Wood TK (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188:305–316. doi:10.1128/JB.188.1.305-316.2006

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  89. Ahmer BM (2004) Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 52:933–945. doi:10.1111/j.1365-2958.2004.04054.x

    Article  PubMed  CAS  Google Scholar 

  90. Wood TK (2009) Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ Microbiol 11:1–15. doi:10.1111/j.1462-2920.2008.01768.x

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  91. Belitsky M, Avshalom H, Erental A, Yelin I, Kumar S, London N, Sperber M, Schueler-Furman O, Engelberg-Kulka H (2011) The Escherichia coli extracellular death factor EDF induces the endoribonucleolytic activities of the toxins MazF and ChpBK. Mol Cell 41:625–635. doi:10.1016/j.molcel.2011.02.023

    Article  PubMed  CAS  Google Scholar 

  92. Zohar BA, Kolodkin-Gal I (2015) Quorum sensing in Escherichia coli: interkingdom, inter- and intraspecies dialogues, and a suicide-inducing peptide. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 85–89. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_9

  93. Walters M, Sperandio V (2006) Autoinducer 3 and epinephrine signaling in the kinetics of locus of enterocyte effacement gene expression in enterohemorrhagic Escherichia coli. Infect Immun 74:5445–5455. doi:10.1128/IAI.00099-06

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  94. Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517–2528. doi:10.1099/00221287-147-9-2517

    Article  PubMed  CAS  Google Scholar 

  95. Venturi V, Friscina A, Bertani I, Devescovi G, Aguilar C (2004) Quorum sensing in the Burkholderia cepacia complex. Res Microbiol 155:238–244. doi:10.1016/j.resmic.2004.01.006

    Article  PubMed  CAS  Google Scholar 

  96. Deng Y, Wu J, Eberl L, Zhang LH (2010) Structural and functional characterization of diffusible signal factor family quorum-sensing signals produced by members of the Burkholderia cepacia complex. Appl Environ Microbiol 76:4675–4683. doi:10.1128/AEM.00480-10

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  97. Patzelt D, Wang H, Buchholz I, Rohde M, Gröbe L, Pradella S, Neumann A, Schulz S, Heyber S, Münch K, Münch R, Jahn D, Wagner-Döbler I, Tomasch J (2013) You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae. ISME J 7:2274–2286. doi:10.1038/ismej.2013.107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  98. Holden MT, Ram Chhabra S, de Nys R, Stead P, Bainton NJ, Hill PJ, Manefield M, Kumar N, Labatte M, England D, Rice S, Givskov M, Salmond GP, Stewart GS, Bycroft BW, Kjelleberg S, Williams P (1999) Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol Microbiol 33:1254–1266. doi:10.1046/j.1365-2958.1999.01577.x

    Article  PubMed  CAS  Google Scholar 

  99. Fraser GM, Bennett JC, Hughes C (1999) Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol Microbiol 32:569–580. doi:10.1046/j.1365-2958.1999.01372.x

    Article  PubMed  CAS  Google Scholar 

  100. Schneider R, Lockatell CV, Johnson D, Belas R (2002) Detection and mutation of a luxS-encoded autoinducer in Proteus mirabilis. Microbiology 148:773–782. doi:10.1099/00221287-148-3-773

    Article  PubMed  CAS  Google Scholar 

  101. Baldo C, Rocha SPD (2014) Virulence factors of uropathogenic Proteus mirabilis—a mini review. Int J Sci Technol Res 3:24–27

    Google Scholar 

  102. Zan J, Cicirelli EM, Mohamed NM, Sibhatu H, Kroll S, Choi O, Uhlson CL, Wysoczynski CL, Murphy RC, Churchill ME, Hill RT, Fuqua C (2012) A complex LuxR–LuxI type quorum sensing network in a roseobacterial marine sponge symbiont activates flagellar motility and inhibits biofilm formation. Mol Microbiol 85:916–933. doi:10.1111/j.1365-2958.2012.08149.x

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  103. Zan J, Liu Y, Fuqua C, Hill RT (2014) Acyl-Homoserine lactone quorum sensing in the Roseobacter clade. Int J Mol Sci 15:654–669. doi:10.3390/ijms15010654

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  104. Taga ME, Miller ST, Bassler BL (2003) Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol Microbiol 50:1411–1427. doi:10.1046/j.1365-2958.2003.03781.x

    Article  PubMed  CAS  Google Scholar 

  105. Choi J, Shin D, Ryu S (2007) Implication of quorum sensing in Salmonella enterica serovar typhimurium virulence: the luxS gene is necessary for expression of genes in pathogenicity island. Infect Immun 75:4885–4890. doi:10.1128/IAI.01942-06

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  106. Atkinson S, Throup JP, Stewart GS, Williams P (1999) A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol Microbiol 33:1267–1277. doi:10.1046/j.1365-2958.1999.01578.x

    Article  PubMed  CAS  Google Scholar 

  107. Bruhn JB, Dalsgaard I, Nielsen KF, Buchholtz C, Larsen JL, Gram L (2005) Quorum sensing signal molecules (acylated homoserine lactones) in gram-negative fish pathogenic bacteria. Dis Aquat Org 65:43–52. doi:10.3354/dao065043

    Article  PubMed  CAS  Google Scholar 

  108. Kastbjerg VG, Nielsen KF, Dalsgaard I, Rasch M, Bruhn JB, Givskov M, Gram L (2007) Profiling acylated homoserine lactones in Yersinia ruckeri and influence of exogenous acyl homoserine lactones and known quorum-sensing inhibitors on protease production. J Appl Microbiol 102:363–374. doi:10.1111/j.1365-2672.2006.03109

    PubMed  CAS  Google Scholar 

  109. Steidle A, Allesen-Holm M, Riedel K, Berg G, Givskov M, Molin S, Eberl L (2002) Identification and characterization of an N-acylhomoserine lactone-dependent quorum-sensing system in Pseudomonas putida strain IsoF. Appl Environ Microbiol 68:6371–6382. doi:10.1128/AEM.68.12.6371-6382.2002

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  110. Bertani I, Venturi V (2004) Regulation of the N-acyl homoserine lactone-dependent quorum-sensing system in rhizosphere Pseudomonas putida WCS358 and cross-talk with the stationary-phase RpoS sigma factor and the global regulator GacA. Appl Environ Microbiol 70:5493–5502. doi:10.1128/AEM.70.9.5493-5502.2004

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  111. Dubern JF, Lugtenberg BJ, Bloemberg GV (2006) The ppuI–rsaL–ppuR quorum-sensing system regulates biofilm formation of Pseudomonas putida PCL1445 by controlling biosynthesis of the cyclic lipopeptides putisolvins I and II. J Bacteriol 188:2898–2906. doi:10.1128/JB.188.8.2898-2906.2006

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  112. Byers JT, Lucas C, Salmond GP, Welch M (2002) Nonenzymatic turnover of an Erwinia carotovora quorum-sensing signaling molecule. J Bacteriol 184:1163–1171. doi:10.1128/jb.184.4.1163-1171.2002

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  113. Barnard AML, Bowden SD, Burr T, Coulthurst SJ, Monson RE, Salmond GPC (2007) Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos Trans R Soc B 362:1165–1183. doi:10.1098/rstb.2007.2042

    Article  CAS  Google Scholar 

  114. Coulthurst SJ, Williamson NR, Harris AK, Spring DR, Salmond GP (2006) Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorum-sensing capacities. Microbiology 152:1899–1911. doi:10.1099/mic.0.28803-0

    Article  PubMed  CAS  Google Scholar 

  115. Christensen AB, Riedel K, Eberl E, Flodgaard LR, Molin S, Gram L, Givskov M (2003) Quorum-sensing-directed protein expression in Serratia proteamaculans B5a. Microbiology 149:471–483. doi:10.1099/mic.0.25575-0

    Article  PubMed  CAS  Google Scholar 

  116. Ovadis M, Liu X, Gavriel S, Ismailov Z, Chet I, Chernin L (2004) The global regulator genes from biocontrol strain Serratia plymuthica IC1270: cloning, sequencing, and functional studies. J Bacteriol 186:4986–4993. doi:10.1128/JB.186.15.4986-4993.2004

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  117. Van Houdt R, Givskov M, Michiels CW (2007) Quorum sensing in Serratia. FEMS Microbiol Rev 31:407–424. doi:10.1111/j.1574-6976.2007.00071.x

    Article  PubMed  CAS  Google Scholar 

  118. Zaĭtseva IuV, Voloshina PV, Liu X, Ovadis MI, Berg G, Chernin LS, Khmel’ IA (2010) Involvement of the global regulators GrrS, RpoS, and SplIR in formation of biofilms in Serratia plymuthica. Genetika 46:616–621

    PubMed  Google Scholar 

  119. Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK, Chhabra SR, Williams P, Macintyre S, Stewart GS (1997) Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 179:5271–5281

    PubMed Central  PubMed  CAS  Google Scholar 

  120. Jangid K, Parameswaran PS, Shouche YS (2012) A variant quorum sensing system in Aeromonas veronii MTCC 3249. Sensors 12:3814–3830. doi:10.3390/s120403814

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  121. Chan XY, How KY, Yin WF, Chan KG (2015) N-acyl homoserine lactone mediated quorum sensing in pathogenic Aeromonas veronii biovar sobria strain 159: identification of LuxIR homologs. PeerJ Prepr 3:e1510. doi:10.7287/peerj.preprints.1232v1

    Article  Google Scholar 

  122. Chu, W, Zhu W and Zhuang X (2015) Quorum sensing systems in Aeromonas spp. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 115–121. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_11

  123. Chan KG, Puthucheary SD, Chan XY, Yin WF, Wong CS, Too WSS, Chua KH (2011) Quorum sensing in Aeromonas species isolated from patients in Malaysia. Curr Microbiol 62:167–172. doi:10.1007/s00284-010-9689-z

    Article  PubMed  CAS  Google Scholar 

  124. White CE, Winans SC (2007) Cell–cell communication in the plant pathogen Agrobacterium tumefaciens. Philos Trans R Soc B 362:1135–1148. doi:10.1098/rstb.2007.2040

    Article  CAS  Google Scholar 

  125. Lang J, Faure D (2014) Functions and regulation of quorum-sensing in Agrobacterium tumefaciens. Front Plant Sci 5:14. doi:10.3389/fpls.2014.00014

    Article  PubMed Central  PubMed  Google Scholar 

  126. Zhu J, Beaber JW, Moré MI, Fuqua C, Eberhard A, Winans SC (1998) Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the traR protein in Agrobacterium tumefaciens. J Bacteriol 180:5398–5405

    PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  128. Genin S, Brito B, Denny TP, Boucher C (2005) Control of the Ralstonia solanacearum Type III secretion system (Hrp) genes by the global virulence regulator PhcA. FEBS Lett 579:2077–2081. doi:10.1016/j.febslet.2005.02.058

    Article  PubMed  CAS  Google Scholar 

  129. Koutsoudis MD, Tsaltas D, Minogue TD, von Bodman SB (2006) Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc Natl Acad Sci USA 103:5983–5988. doi:10.1073/pnas.0509860103

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  130. Tan JY, Yin WF, Chan KG (2014) Quorum sensing activity of Hafnia alvei isolated from packed food. Sensors 14:6788–6796. doi:10.3390/s140406788

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  131. Chalupowicz L, Barash I, Panijel M, Sessa G, Manulis-Sasson S (2008) Regulatory interactions between quorum-sensing, auxin, cytokinin, and the Hrp regulon in relation to gall formation and epiphytic fitness of Pantoea agglomerans pv. gypsophilae. MPMI 22:849–856. doi:10.1094/MPMI-22-7-0849

    Article  CAS  Google Scholar 

  132. Bhargava N, Sharma P, Capalash N (2010) Quorum sensing in Acinetobacter: an emerging pathogen. Crit Rev Microbiol 36:349–360. doi:10.3109/1040841X.2010.512269

    Article  PubMed  CAS  Google Scholar 

  133. Terwagne M, Mirabella A, Lemaire J, Deschamps C, De Bolle X, Letesson JJ (2013) Quorum sensing and self-quorum quenching in the intracellular pathogen Brucella melitensis. PLoS One 8:e82514. doi:10.1371/journal.pone.0082514

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  134. Bhargava N, Sharma P, Capalash N (2015) Quorum sensing in Acinetobacter baumannii. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 101–113. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_10

  135. Paggi RA, Martone CB, Fuqua C, De Castro RE (2003) Detection of quorum sensing signals in the haloalkaliphilic archaeon Natronococcus occultus. FEMS Microbiol Lett 221:49–52. doi:10.1016/S0378-1097(03)00174-5

    Article  PubMed  CAS  Google Scholar 

  136. Llamas I, Quesada E, Martinez-Canovas MJ, Gronquist M, Eberhard A, Gonzalez JE (2005) Quorum sensing in halophilic bacteria: detection of N-acyl-homoserine lactones in the exopolysaccharide-producing species of Halomonas. Extremophiles 9:333–341. doi:10.1007/s00792-005-0448-1

    Article  PubMed  CAS  Google Scholar 

  137. Tahrioui A, Quesada E, Llamas I (2011) The hanR/hanI quorum-sensing system of Halomonas anticariensis, a moderately halophilic bacterium. Microbiology 157:3378–3387. doi:10.1099/mic.0.052167-0

    Article  PubMed  CAS  Google Scholar 

  138. Johnson MR, Montero CI, Conners SB, Shockley KR, Bridger SL, Kelly RM (2005) Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga maritima. Mol Microbiol 55:664–674. doi:10.1111/j.1365-2958.2004.04419.x

    Article  PubMed  CAS  Google Scholar 

  139. Sun J, Daniel R, Wagner-Döbler I, Zeng AP (2004) Is autoinducer-2 a universal signal for interspecies communication: a comparative genomic and phylogenetic analysis of the synthesis and signal transduction pathways. BMC Evol Biol 4:36. doi:10.1186/1471-2148-4-36

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  140. Day WA Jr, Maurelli AT (2001) Shigella flexneri LuxS quorum-sensing system modulates virB expression but is not essential for virulence. Infect Immun 69:15–23. doi:10.1128/IAI.69.1.15-23.2001

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  141. Balestrino D, Haagensen JAJ, Rich C, Forestier C (2005) Characterization of type 2 quorum sensing in Klebsiella pneumoniae and relationship with biofilm formation. J Bacteriol 187:2870–2880. doi:10.1128/JB.187.8.2870-2880.2005

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  142. He YW, Boon C, Zhou L, Zhang LH (2009) Co-regulation of Xanthomonas campestris virulence by quorum sensing and a novel two-component regulatory system RavS/RavR. Mol Microbiol 71:1464–1476. doi:10.1111/j.1365-2958.2009.06617.x

    Article  PubMed  CAS  Google Scholar 

  143. Hirakawa H, Oda Y, Phattarasukol S, Armour CD, Castle JC, Raymond CK, Lappala CR, Schaefer AL, Harwood CS, Greenberg EP (2011) Activity of the Rhodopseudomonas palustris p-coumaroyl-homoserine lactone-responsive transcription factor RpaR. J Bacteriol 193:2598–2607. doi:10.1128/JB.01479-10

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  144. Rader BA, Wreden C, Hicks KG, Sweeney EG, Ottemann KM, Guillemin K (2011) Helicobacter pylori perceives the quorum-sensing molecule AI-2 as a chemorepellent via the chemoreceptor TlpB. Microbiology 157:2445–2455. doi:10.1099/mic.0.049353-0

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  145. Scheres N, Lamont RJ, Crielaard W, Krom BP (2015) LuxS signaling in Porphyromonas gingivalis-host interactions. Anaerobe 35:3–9. doi:10.1016/j.anaerobe.2014.11.011

    Article  PubMed  CAS  Google Scholar 

  146. Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drug targets. Crit Rev Microbiol 37:121–140. doi:10.3109/1040841X.2010.532479

    Article  PubMed  CAS  Google Scholar 

  147. Kalia VC, Wood TK, Kumar P (2014) Evolution of resistance to quorum-sensing inhibitors. Microb Ecol 68:13–23. doi:10.1007/s00248-013-0316-y

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  148. Nusrat H, Kushwah J, Joshi J, Raju SC, Kalia VC (2011) Diversity and polymorphism in AHL-lactonase gene (aiiA) of Bacillus. J Microbiol Biotechnol 21:1001–1011. doi:10.4014/jmb.1105.05056

    Article  CAS  Google Scholar 

  149. Kalia VC, Raju SC, Purohit HJ (2011) Genomic analysis reveals versatile organisms for quorum quenching enzymes: acyl-homoserine lactone-acylase and-lactonase. Open Microbiol J 5:1–11. doi:10.2174/1874285801105010001

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  150. Kumar P, Patel SK, Lee J-K, Kalia VC (2013) Extending the limits of Bacillus for novel biotechnological applications. Biotechnol Adv 31:1543–1561. doi:10.1016/j.biotechadv.2013.08.007

    Article  PubMed  CAS  Google Scholar 

  151. Sarabhai S, Sharma P, Capalash N (2013) Ellagic acid derivatives from Terminalia chebula Retz. downregulate the expression of quorum sensing genes to attenuate Pseudomonas aeruginosa PAO1 virulence. PLoS One 8:e53441. doi:10.1371/journal.pone.0053441

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  152. Kumar P, Koul S, Patel SK, Lee J-K, Kalia VC (2015) Heterologous expression of quorum sensing inhibitory genes in diverse organisms. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 343-356. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_28

  153. Czajkowski R, Jafra S (2009) Quenching of acylhomoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol 56:1–16

    PubMed  CAS  Google Scholar 

  154. Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116. doi:10.1021/cr100045m

    Article  PubMed  CAS  Google Scholar 

  155. Kalia VC, Kumar P (2015) Potential applications of quorum sensing inhibitors in diverse fields. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 359–370. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_29

  156. Kalia VC, Kumar P, Pandian SK, Sharma P (2015) Biofouling control by quorum quenching. In: Kim S-K (ed) Hb25_Springer Handbook of Marine Biotechnology. Springer, Berlin, pp 431–440. doi:10.1007/978-3-642-53971-8_15

    Chapter  Google Scholar 

  157. Kalia VC, Rani A, Lal S, Cheema S, Raut CP (2007) Combing databases reveals potential antibiotic producers. Expert Opin Drug Discov 2:211–224. doi:10.1517/17460441.2.2.211

    Article  PubMed  CAS  Google Scholar 

  158. Purohit HJ, Cheema S, Lal S, Raut CP, Kalia VC (2007) In search of drug targets for Mycobacterium tuberculosis. Infect Disord Drug Targets 7:245–250. doi:10.2174/187152607782110068

    Article  PubMed  CAS  Google Scholar 

  159. Saxena A, Mukherjee M, Kumari R, Singh P, Lal R (2014) Synthetic biology in action: developing a drug against MDR-TB. Indian J Microbiol 54:369–375. doi:10.1007/s12088-014-0498-0

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  161. García-Contreras R, Martinez-Vazquez M, Velazquez Guadarrama N, Villegas Paneda AG, Hashimoto T, Maeda T, Quezada H, Wood TK (2013) Resistance to the quorum-quenching compounds brominated furanone C-30 and 5-fluorouracil in Pseudomonas aeruginosa clinical isolates. Pathog Dis 68:8–11. doi:10.1111/2049-632X.12039

    Article  PubMed  CAS  Google Scholar 

  162. Kalia VC, Kumar P (2015) The battle: quorum-sensing inhibitors versus evolution of bacterial resistance. In: Kalia VC (ed) Quorum sensing vs quorum quenching: a battle with no end in sight, pp 385–391. Springer India. ISBN 978-81-322-1981-1. doi:10.1007/978-81-322-1982-8_31

  163. Lerat E, Moran NA (2004) The evolutionary history of quorum-sensing systems in bacteria. Mol Biol Evol 21:903–913. doi:10.1093/molbev/msh097

    Article  PubMed  CAS  Google Scholar 

  164. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222. doi:10.1146/annurev-genet-102108-134304

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  165. Case RJ, Labbate M, Kjelleberg S (2008) AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J 2:345–349. doi:10.1038/ismej.2008.13

    Article  PubMed  CAS  Google Scholar 

  166. Lee JH, Lequette Y, Greenberg EP (2006) Activity of purified QscR, a Pseudomonas aeruginosa orphan quorum-sensing transcription factor. Mol Microbiol 59:602–609. doi:10.1111/j.1365-2958.2005.04960.x

    Article  PubMed  CAS  Google Scholar 

  167. Shang Z, Wang H, Zhou S, Chu W (2014) Characterization of N-acyl-homoserine lactones (AHLs)-deficient clinical isolates of Pseudomonas aeruginosa. Indian J Microbiol 54:158–162. doi:10.1007/s12088-014-0449-9

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  168. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415:545–549. doi:10.1038/415545a

    Article  PubMed  CAS  Google Scholar 

  169. Duan F, March JC (2008) Interrupting Vibrio cholerae infection of human epithelial cells with engineered commensal bacterial signaling. Biotechnol Bioeng 101:128–134. doi:10.1002/bit.21897

    Article  PubMed  CAS  Google Scholar 

  170. Horng YT, Deng SC, Daykin M, Soo PC, Wei JR, Luh KT, Ho SW, Swift S, Lai HC, Williams P (2002) The LuxR family protein SpnR functions as a negative regulator of N-acylhomoserine lactone-dependent quorum sensing in Serratia marcescens. Mol Microbiol 45:1655–1671. doi:10.1046/j.1365-2958.2002.03117.x

    Article  PubMed  CAS  Google Scholar 

  171. Jahan N, Potter JA, Sheikh MA, Botting CH, Shirran SL, Westwood NJ, Taylor GL (2009) Insights into the biosynthesis of the Vibrio cholerae major autoinducer CAI-1 from the crystal structure of the PLP-dependent enzyme CqsA. J Mol Biol 392:763–773. doi:10.1016/j.jmb.2009.07.042

    Article  PubMed  CAS  Google Scholar 

  172. Krell T, Lacal J, Busch A, Silva-Jime´nez H, Guazzaroni M-E, Ramos JL (2010) Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64:539–559. doi:10.1146/annurev.micro.112408.134054

    Article  PubMed  CAS  Google Scholar 

  173. Boedicke JQ, Vincent ME, Ismagilov RF (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 Engl 48:5908–5911. doi:10.1002/anie.200901550

    Article  CAS  Google Scholar 

  174. Kalia VC, Lal S, Cheema S (2007) Insight into the phylogeny of polyhydroxyalkanoate biosynthesis: horizontal gene transfer. Gene 389:19–26. doi:10.1016/j.gene.2006.09.010

    Article  PubMed  CAS  Google Scholar 

  175. Lal S, Cheema S, Kalia VC (2008) Phylogeny vs genome reshuffling: horizontal gene transfer. Indian J Microbiol 48:228–242. doi:10.1007/s12088-008-0034-1

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  176. Darch SE, West SA, Winzer K, Diggle SP (2012) Density-dependent fitness benefits in quorum-sensing bacterial populations. Proc Natl Acad Sci USA 109:8259–8263. doi:10.1073/pnas.1118131109

    Article  PubMed Central  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are thankful to the Director of CSIR - Institute of Genomics and Integrative Biology (IGIB), and CSIR project INDEPTH (BSC0111) for providing the necessary funds, facilities and moral support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shikha Koul.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koul, S., Prakash, J., Mishra, A. et al. Potential Emergence of Multi-quorum Sensing Inhibitor Resistant (MQSIR) Bacteria. Indian J Microbiol 56, 1–18 (2016). https://doi.org/10.1007/s12088-015-0558-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-015-0558-0

Keywords

Navigation