Enzymatic Quorum Quenching for Virulence Attenuation of Phytopathogenic Bacteria

  • Ashtaad Vesuna
  • Anuradha S. Nerurkar


Quorum sensing is a process of cell-cell communication by which the bacteria vary their gene expression mediated by a self-produced signalling molecule in a population density dependent manner to coordinate their behaviour which is virulence in phytopathogens. Quorum quenching or quorum sensing inhibition is a broad term used to include many diverse mechanisms that interfere with the quorum sensing signalling where signal degrading enzymes comprise one of the important mechanism. The signalling molecule, AHL (N-acyl homoserine lactone) is central to the process of quorum sensing in many Gram negative phytopathogenic bacteria. With constant rise in the number of resistant bacterial pathogens, enzymatic quorum quenching is an effective alternative way to attenuate their virulence. Quorum quenching does not kill the pathogen but stops its quorum sensing activity and thus does not introduce selective pressure which leads to development of resistance. Quorum sensing signal degrading strategy can thus be an effective means of biocontrol of phytopathogens. This chapter briefly discusses the virulence processes mediated by quorum sensing in Gram negative plant pathogens particularly in Pectobacterium carotovorum subsp. carotovorum. and their virulence attenuation by AHL degrading enzymes such as lactonases, acylases and oxido-reductases produced by various bacteria including Actinobacteria. The main focus is on enzymes produced by the quorum quenching bacteria, the genes that control the enzymes and the mechanism by which they attenuate quorum sensing mediated virulence in Gram negative phytopathogenic bacteria.


Quorum sensing Quorum quenching Phytopathogens N-acyl Homoserine lactone 



N-acylhomoserine lactone


N-butanoyl-L-homoserine lactone,


















Homoserine lactone,


Pectobacterium carotovorum subsp. carotovorum,


Plant Cell Wall Degrading Enzyme


Quorum Sensing,


Quorum Quenching,


Quorum sensing Inhibitor


  1. Arumugam K, Ramalingam P, Appu M (2017) Isolation of Trichoderma viride and Pseudomonas fluorescens organism from soil and their treatment against rice pathogens. J Microbiol 3:77–81Google Scholar
  2. Bassler BL (2002) Small talk: cell-to-cell communication in bacteria. Cell 109:421–424. CrossRefPubMedGoogle Scholar
  3. Biancalani C, Cerboneschi M, Tadini-Buoninsegni F, Campo M, Scardigli A, Romani A, Tegli S (2016) Global analysis of type three secretion system and quorum sensing inhibition of Pseudomonas savastanoi by polyphenols extracts from vegetable residues. PLoS One 11:e0163357. CrossRefPubMedCentralPubMedGoogle Scholar
  4. Bondí R, Longo F, Messina M, D’Angelo F, Visca P, Leoni L, Rampioni G (2017) The multi-output incoherent feed forward loop constituted by the transcriptional regulators LasR and RsaL confers robustness to a subset of quorum sensing genes in Pseudomonas aeruginosa. Mol BioSyst 13:1080–1089. CrossRefPubMedGoogle Scholar
  5. Borges A, Serra S, Cristina Abreu A, Saavedra MJ, Salgado A, Simões M (2014) Evaluation of the effects of selected phytochemicals on quorum sensing inhibition and in vitro cytotoxicity. Biofouling 30:183–195. CrossRefPubMedGoogle Scholar
  6. Bowden SD, Hale N, Chung JC, Hodgkinson JT, Spring DR, Welch M (2013) Surface swarming motility by Pectobacterium atrosepticum is a latent phenotype that requires O antigen and is regulated by quorum sensing. Microbiology 159:2375–2385. CrossRefPubMedGoogle Scholar
  7. Boyer M, Wisniewski-Dyé F (2009) Cell–cell signaling in bacteria: not simply a matter of quorum. ISME J 70:1–19. CrossRefGoogle Scholar
  8. Burke AK, Duong DA, Jensen RV, Stevens AM (2015) Analyzing the transcriptomes of two quorum-sensing controlled transcription factors, RcsA and LrhA, important for Pantoea stewartii virulence. PLoS One 10:e0145358. CrossRefGoogle Scholar
  9. Cai Z, Yuan ZH, Zhang H, Pan Y, Wu Y, Tian XQ, Wang FF, Wang L, Qian W (2017) Fatty acid DSF binds and allosterically activates histidine kinase RpfC of phytopathogenic bacterium Xanthomonas campestris pv. campestris to regulate quorum-sensing and virulence. PLoS Pathog 13:e1006304. CrossRefPubMedCentralPubMedGoogle Scholar
  10. Chan KG, Atkinson S, Mathee K, Sam CK, Chhabra SR, Cámara M et al (2011) Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale (ginger) rhizosphere: co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia. BMC Microbiol 11:51. CrossRefPubMedCentralPubMedGoogle Scholar
  11. Chang CY, Krishnan T, Wang H, Chen Y, Yin WF, Chong YM, Tan LY, Chong TM, Chan KG (2014) Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone synthase as druggable target. Sci Rep 4:7245. CrossRefPubMedCentralPubMedGoogle Scholar
  12. Chen CN, Chen CJ, Liao CT, Lee CY (2009) A probable aculeacin A acylase from the Ralstonia solanacearum GMI1000 is N-acyl-homoserine lactone acylase with quorum-quenching activity. BMC Microbiol 9:89. CrossRefPubMedCentralPubMedGoogle Scholar
  13. Chen F, Gao Y, Chen X, Yu Z, Li X (2013) Quorum quenching enzymes and their application in degrading signal molecules to block quorum sensing-dependent infection. Int J Mol Sci 14:17477–17500. CrossRefPubMedCentralPubMedGoogle Scholar
  14. Chen R, Barphagha IK, Ham JH (2015) Identification of potential genetic components involved in the deviant quorum-sensing signaling pathways of Burkholderia glumae through a functional genomics approach. Front Cell Infect Microbiol 5:22. CrossRefPubMedCentralPubMedGoogle Scholar
  15. Cirou A, Diallo S, Kurt C, Latour X, Faure D (2007) Growth promotion of quorum-quenching bacteria in the rhizosphere of Solanum tuberosum. Environ Microbiol 9:1511–1522. CrossRefPubMedGoogle Scholar
  16. Cirou A, Mondy S, An S, Charrier A, Sarrazin A, Thoison O, Faure D (2012) Efficient biostimulation of native and introduced quorum-quenching Rhodococcus erythropolis populations is revealed by a combination of analytical chemistry, microbiology, and pyrosequencing. Appl Environ Microbiol 78:481–492. CrossRefPubMedCentralPubMedGoogle Scholar
  17. Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci USA 111:4280–4284. CrossRefPubMedCentralPubMedGoogle Scholar
  18. Cui X, Harling R (2005) N-acyl-homoserine lactone-mediated quorum sensing blockage, a novel strategy for attenuating pathogenicity of Gram-negative bacterial plant pathogens. Eur J Plant Pathol 111:327–339. CrossRefGoogle Scholar
  19. Cui Y, Chatterjee A, Liu Y, Dumenyo CK, Chatterjee AK (1995) Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J Bacteriol 177:5108–5115. CrossRefPubMedCentralPubMedGoogle Scholar
  20. Cui Y, Chatterjee A, Hasegawa H, Dixit V, Leigh N, Chatterjee AK (2005) ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J Bacteriol 187:4792–4803.–4803.2005 CrossRefPubMedCentralPubMedGoogle Scholar
  21. Czajkowski R, Krzyżanowska D, Karczewska J, Atkinson S, Przysowa J, Lojkowska E, Jafra S (2011) Inactivation of AHLs by Ochrobactrum sp. A44 depends on the activity of a novel class of AHL acylase. Environ Microbiol Rep 3:59–68. CrossRefPubMedGoogle Scholar
  22. De Simone M, Spagnuolo L, Lorè NI, Rossi G, Cigana C, De Fino I, Iraqi FA, Bragonzi A (2014) Host genetic background influences the response to the opportunistic Pseudomonas aeruginosa infection altering cell-mediated immunity and bacterial replication. PLoS One 9:e106873. CrossRefPubMedCentralPubMedGoogle Scholar
  23. Defoirdt T, Brackman G, Coenye T (2013) Quorum sensing inhibitors: how strong is the evidence? Trends Microbiol 21:619–624. CrossRefGoogle Scholar
  24. Des Essarts YR, Cigna J, Quêtu-Laurent A, Caron A, Munier E, Beury-Cirou A et al (2016) Biocontrol of the potato blackleg and soft rot diseases caused by Dickeya dianthicola. Appl Environ Microbiol 82:268–278. CrossRefGoogle Scholar
  25. Dong YH, Zhang LH (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43:101–109PubMedGoogle Scholar
  26. Dong YH, Wang LH, Xu JL, Zhang HB (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813. CrossRefPubMedGoogle Scholar
  27. Du Y, Li T, Wan Y, Liao P (2014) Signal molecule-dependent quorum-sensing and quorum-quenching enzymes in bacteria. Crit Rev Eukaryot Gene Expr 24:117–132. CrossRefPubMedGoogle Scholar
  28. Fetzner S (2015) Quorum quenching enzymes. J Biotechnol 201:2–14. CrossRefPubMedGoogle Scholar
  29. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gao R, Krysciak D, Petersen K, Utpatel C, Knapp A, Schmeisser C, Daniel R, Voget S, Jaeger KE, Streit WR (2015) Genome-wide RNA sequencing analysis of quorum sensing-controlled regulons in the plant-associated Burkholderia glumae PG1 strain. Appl Environ Microbiol 81:7993–8007. CrossRefPubMedCentralPubMedGoogle Scholar
  31. García-Lara B, Saucedo-Mora MÁ, Roldán-Sánchez JA, Pérez-Eretza B, Ramasamy M, Lee J, Coria-Jimenez R, Tapia M, Varela-Guerrero V, García-Contreras R (2015) Inhibition of quorum-sensing-dependent virulence factors and biofilm formation of clinical and environmental Pseudomonas aeruginosa strains by ZnO nanoparticles. Lett Appl Microbiol 61:299–305. CrossRefPubMedGoogle Scholar
  32. Garge SS, Nerurkar AS (2016) Attenuation of quorum sensing regulated virulence of Pectobacterium carotovorum subsp. carotovorum through an AHL lactonase produced by Lysinibacillus sp. Gs50. PLoS One 11:e0167344. CrossRefPubMedCentralPubMedGoogle Scholar
  33. Garge SS, Nerurkar AS (2017) Evaluation of quorum quenching Bacillus spp. for their biocontrol traits against Pectobacterium carotovorum subsp. carotovorum causing soft rot. Biocatal Agric Biotechnol 9:48–57. CrossRefGoogle Scholar
  34. Grandclément C, Tannières M, Moréra S, Dessaux Y, Faure D (2015) Quorum quenching: role in nature and applied developments. FEMS Microbiol Lett 40:86–116. CrossRefGoogle Scholar
  35. Ham JH (2013) Intercellular and intracellular signalling systems that globally control the expression of virulence genes in plant pathogenic bacteria. Mol Plant Pathol 14:308–322. CrossRefPubMedGoogle Scholar
  36. Helman Y, Chernin L (2015) Silencing the mob: disrupting quorum sensing as a means to fight plant disease. Mol Plant Pathol 16:316–329. CrossRefPubMedGoogle Scholar
  37. Hilker R, Munder A, Klockgether J, Losada PM, Chouvarine P, Cramer N, Davenport CF, Dethlefsen S, Fischer S, Peng H, Schönfelder T (2015) Interclonal gradient of virulence in the Pseudomonas aeruginosa pangenome from disease and environment. Environ Microbiol 17:29–46. CrossRefPubMedGoogle Scholar
  38. Høyland-Kroghsbo NM, Paczkowski J, Mukherjee S, Broniewski J, Westra E, Bondy-Denomy J, Bassler BL (2016) Quorum sensing controls the Pseudomonas aeruginosa CRISPR-Cas adaptive immune system. Proc Natl Acad Sci USA 114:131–135. CrossRefPubMedCentralPubMedGoogle Scholar
  39. Huma N, Shankar P, Kushwah J, Bhushan A, Joshi J, Mukherjee T, Raju SC, Purohit HJ, Kalia VC (2011) Diversity and polymorphism in AHL-lactonase gene (aiiA) of Bacillus. J Microbiol Biotechnol 21:1001–1011. CrossRefPubMedGoogle Scholar
  40. Ihekwaba AE, Mura I, Peck MW, Barker GC (2015) The pattern of growth observed for Clostridium botulinum type A1 strain ATCC 19397 is influenced by nutritional status and quorum sensing: a modelling perspective. FEMS Pathogens Dis 73:ftv084. CrossRefGoogle Scholar
  41. Ishii S, Fukui K, Yokoshima S, Kumagai K, Beniyama Y, Kodama T, Fukuyama T, Okabe T, Nagano T, Kojima H, Yano T (2017) High throughput screening of small molecule inhibitors of the Streptococcus quorum-sensing signal pathway. Sci Rep 7:4029. CrossRefPubMedCentralPubMedGoogle Scholar
  42. Jacquet P, Daudé D, Bzdrenga J, Masson P, Elias M, Chabrière E (2016) Current and emerging strategies for organophosphate decontamination: special focus on hyperstable enzymes. Environ Sci Pollut Res 23:8200–8218. CrossRefGoogle Scholar
  43. Jang MS, Goo E, An JH, Kim J, Hwang I (2014) Quorum sensing controls flagellar morphogenesis in Burkholderia glumae. PLoS One 9:e84831. CrossRefPubMedCentralPubMedGoogle Scholar
  44. Joshi JR, Khazanov N, Senderowitz H, Burdman S, Lipsky A, Yedidia I (2016) Plant phenolic volatiles inhibit quorum sensing in pectobacteria and reduce their virulence by potential binding to ExpI and ExpR proteins. Sci Rep 6:38126. CrossRefPubMedCentralPubMedGoogle Scholar
  45. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31:224–245. CrossRefPubMedCentralPubMedGoogle Scholar
  46. Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drug targets. Crit Rev Microbiol 37:121–140. CrossRefPubMedCentralPubMedGoogle Scholar
  47. 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 5:1–13. CrossRefPubMedCentralPubMedGoogle Scholar
  48. Khoiri S, Damayanti TA, Giyanto G (2017) Identification of quorum quenching bacteria and its biocontrol potential against soft rot disease bacteria, Dickeya dadantii. Agrivita 39:45. CrossRefGoogle Scholar
  49. Koch B, Liljefors T, Persson T, Nielsen J, Kjelleberg S, Givskov M (2005) The LuxR receptor: the sites of interaction with quorum-sensing signals and inhibitors. Microbiol 151:3589–3602. CrossRefGoogle Scholar
  50. Koul S, Kalia VC (2017) Multiplicity of quorum quenching enzymes: a potential mechanism to limit quorum sensing bacterial population. Indian J Microbiol 57:100–108. CrossRefPubMedCentralPubMedGoogle Scholar
  51. Krysciak D, Schmeisser C, Preuss S, Riethausen J, Quitschau M, Grond S, Streit WR (2011) Involvement of multiple loci in quorum quenching of autoinducer I molecules in the nitrogen-fixing symbiont Rhizobium (Sinorhizobium) sp. strain NGR234. Appl Environ Microbiol 77:5089–5099. CrossRefPubMedCentralPubMedGoogle Scholar
  52. Lang J, Faure D (2014) Functions and regulation of quorum-sensing in Agrobacterium tumefaciens. Front Plant Sci 5:14. CrossRefPubMedCentralPubMedGoogle Scholar
  53. Latour X, Barbey C, Chane A, Groboillot A, Burini JF (2013) Rhodococcus erythropolis and its γ-lactone catabolic pathway: an unusual biocontrol system that disrupts pathogen quorum sensing communication. Agronomy 3:816–838. CrossRefGoogle Scholar
  54. Lee J, Zhang L (2015) The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41. CrossRefPubMedCentralPubMedGoogle Scholar
  55. Lee DH, Lim JA, Lee J, Roh E, Jung K, Choi M, Oh C, Ryu S, Yun J, Heu S (2013) Characterization of genes required for the pathogenicity of Pectobacterium carotovorum subsp. carotovorum Pcc21 in Chinese cabbage. Microbiology 159:1487–1496. CrossRefPubMedCentralPubMedGoogle Scholar
  56. Liang X, Yu X, Pan X, Wu J, Duan Y, Wang J, Zhou M (2016) A thiadiazole reduces the virulence of Xanthomonas oryzae pv. oryzae by inhibiting the histidine utilization pathway and quorum sensing. Mol Plant Pathol.
  57. Liu CF, Liu D, Momb J, Thomas PW, Lajoie A, Petsko GA, Fast W, Ringe D (2013) A phenylalanine clamp controls substrate specificity in the quorum-quenching metallo-γ-lactonase from Bacillus thuringiensis. Biochemistry 52:1603–1610. CrossRefPubMedCentralPubMedGoogle Scholar
  58. Loh J, Pierson EA, Pierson LS, Stacey G, Chatterjee A (2002) Quorum sensing in plant-associated bacteria. Curr Opin Plant Biol 5:285–290. 12179960 CrossRefPubMedGoogle Scholar
  59. Maisuria VB, Nerurkar AS (2012) Biochemical properties and thermal behaviour of pectate lyase produced by Pectobacterium carotovorum subsp. carotovorum BR1 with industrial potentials. Biochem Eng J 63:22–30. CrossRefGoogle Scholar
  60. Maisuria VB, Nerurkar AS (2013) Characterization and differentiation of soft rot causing Pectobacterium carotovorum of Indian origin. Eur J Plant Pathol 136:87–102. CrossRefGoogle Scholar
  61. Maisuria VB, Nerurkar AS (2015) Interference of quorum sensing by Delftia sp. VM4 depends on the activity of a novel N-Acylhomoserine lactone-acylase. PLoS One 10:e0138034. CrossRefPubMedCentralPubMedGoogle Scholar
  62. Maisuria VB, Patel VA, Nerurkar AS (2010) Biochemical and thermal stabilization parameters of polygalacturonase from Erwinia carotovora subsp. carotovora BR1. J Microbiol Biotechnol 20:1077–1085. 20668400 CrossRefPubMedGoogle Scholar
  63. Maisuria VB, Lopez-de Los Santos Y, Tufenkji N, Déziel E (2016) Cranberry-derived proanthocyanidins impair virulence and inhibit quorum sensing of Pseudomonas aeruginosa. Sci Rep 6:30169. CrossRefPubMedCentralPubMedGoogle Scholar
  64. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P et al (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629. CrossRefPubMedGoogle Scholar
  65. McCann HC, Rikkerink EH, Bertels F, Fiers M, Lu A, Rees-George J, Andersen MT, Gleave AP, Haubold B, Wohlers MW, Guttman DS (2013) Genomic analysis of the kiwifruit pathogen Pseudomonas syringae pv. actinidiae provides insight into the origins of an emergent plant disease. PLoS Pathog 9:e1003503. CrossRefPubMedCentralPubMedGoogle Scholar
  66. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199. CrossRefPubMedGoogle Scholar
  67. Mole BM, Baltrus DA, Dangl JL, Grant SR (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol 15:363–371. CrossRefPubMedGoogle Scholar
  68. Moleleki LN, Pretorius RG, Tanui CK, Mosina G, Theron J (2017) A quorum sensing-defective mutant of Pectobacterium carotovorum ssp. brasiliense 1692 is attenuated in virulence and unable to occlude xylem tissue of susceptible potato plant stems. Mol Plant Pathol 18:32–44. CrossRefPubMedGoogle Scholar
  69. Monson R, Burr T, Carlton T, Liu H, Hedley P, Toth I, Salmond GP (2013) Identification of genes in the VirR regulon of Pectobacterium atrosepticum and characterization of their roles in quorum sensing-dependent virulence. Environ Microbiol Rep 15:687–701. CrossRefGoogle Scholar
  70. Mori Y, Ishikawa S, Ohnishi H, Shimatani M, Morikawa Y, Hayashi K, Hikichi Y (2017) Involvement of ralfuranones in the quorum sensing signalling pathway and virulence of Ralstonia solanacearum strain OE1-1. Mol Plant Pathol.
  71. Morohoshi T, Tominaga Y, Someya N, Ikeda T (2012) Complete genome sequence and characterization of the N-acylhomoserine lactonedegrading gene of the potato leaf-associated Solibacillus silvestris. J Biosci Bioeng 113(1):20–25. CrossRefPubMedGoogle Scholar
  72. Mukherjee S, Moustafa D, Smith CD, Goldberg JB, Bassler BL (2017) The RhlR quorum-sensing receptor controls Pseudomonas aeruginosa pathogenesis and biofilm development independently of its canonical homoserine lactone autoinducer. PLoS Pathog 13:e1006504. CrossRefPubMedCentralPubMedGoogle Scholar
  73. Nasser W, Dorel C, Wawrzyniak J, Van Gijsegem F, Groleau MC, Déziel E, Reverchon S (2013) Vfm a new quorum sensing system controls the virulence of Dickeya dadantii. Environ Microbiol 15:865–880. CrossRefPubMedGoogle Scholar
  74. Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–322PubMedCentralPubMedGoogle Scholar
  75. Newton JA, Fray RG (2004) Integration of environmental and host-derived signals with quorum sensing during plant–microbe interactions. Cell Microbiol 6:213–224. CrossRefPubMedGoogle Scholar
  76. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222. CrossRefPubMedCentralPubMedGoogle Scholar
  77. Nickzad A, Lépine F, Déziel E (2015) Quorum sensing controls swarming motility of Burkholderia glumae through regulation of rhamnolipids. PLoS One 10:e0128509. CrossRefPubMedCentralPubMedGoogle Scholar
  78. O’Rourke JP, Daly SM, Triplett KD, Peabody D, Chackerian B, Hall PR (2014) Development of a mimotope vaccine targeting the Staphylococcus aureus quorum sensing pathway. PLoS One 9:e111198. CrossRefPubMedCentralPubMedGoogle Scholar
  79. Papenfort K, Bassler BL (2016) Quorum sensing signal-response systems in gram-negative bacteria. Nat Rev Microbiol 14:576–588. CrossRefPubMedCentralPubMedGoogle Scholar
  80. Park SY, Lee SJ, Oh TK, Oh JW, Koo BT, Yum DY, Lee JK (2003) AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149:1541–1550. CrossRefPubMedGoogle Scholar
  81. Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY (2005) Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microbiol 71:2632–2641.–2641.2005 CrossRefPubMedCentralPubMedGoogle Scholar
  82. Pérez-Velázquez J, Quiñones B, Hense BA, Kuttler C (2015) A mathematical model to investigate quorum sensing regulation and its heterogeneity in Pseudomonas syringae on leaves. Ecol Complex 21:128–141. CrossRefGoogle Scholar
  83. Polkade AV, Mantri SS, Patwekar UJ, Jangid K (2016) Quorum sensing: an under-explored phenomenon in the phylum Actinobacteria. Front Microbiol 7:131. CrossRefPubMedCentralPubMedGoogle Scholar
  84. Põllumaa L, Alamäe T, Mäe A (2012) Quorum sensing and expression of virulence in Pectobacteria. Sensors 12:3327–3349. CrossRefPubMedCentralPubMedGoogle Scholar
  85. Qi J, Li L, Du Y, Wang S, Wang J, Luo Y, Che J, Lu J, Liu H, Hu G, Li J (2014) The identification, typing, and antimicrobial susceptibility of Pseudomonas aeruginosa isolated from mink with hemorrhagic pneumonia. Vet Microbiol 170:456–461. CrossRefPubMedGoogle Scholar
  86. Rajesh PS, Rai VR (2016) Inhibition of QS-regulated virulence factors in Pseudomonas aeruginosa PAO1 and Pectobacterium carotovorum by AHL-lactonase of endophytic bacterium Bacillus cereus VT96. Biocatal Agric Biotechnol 7:154–163. CrossRefGoogle Scholar
  87. Ramachandran R, Stevens AM (2013) Proteomic analysis of the quorum-sensing regulon in Pantoea stewartii and identification of direct targets of EsaR. Appl Environ Microbiol 79:6244–6252. CrossRefPubMedCentralPubMedGoogle Scholar
  88. Ramachandran R, Burke AK, Cormier G, Jensen RV, Stevens AM (2014) Transcriptome-based analysis of the Pantoea stewartii quorum-sensing regulon and identification of EsaR direct targets. Appl Environ Microbiol 80:5790–5800. CrossRefPubMedCentralPubMedGoogle Scholar
  89. Riaz K, Elmerich C, Moreira D, Raffoux A, Dessaux Y, Faure D (2008) A metagenomic analysis of soil bacteria extends the diversity of quorum quenching lactonases. Environ Microbiol 10:560–570. CrossRefPubMedGoogle Scholar
  90. Rizzello CG, Filannino P, Di Cagno R, Calasso M, Gobbetti M (2014) Quorum-sensing regulation of constitutive plantaricin by Lactobacillus plantarum strains under a model system for vegetables and fruits. Appl Environ Microbiol 80:777–787. CrossRefPubMedCentralPubMedGoogle Scholar
  91. Rolland J, Stien D, Sanchez-Ferandin S, Lami R (2016) Quorum sensing and quorum quenching in the phycosphere of phytoplankton: a case of chemical interactions in ecology. J Chem Ecol 42:1201–1211. CrossRefPubMedGoogle Scholar
  92. Romero M, Diggle SP, Heeb S, Camara M, Otero A (2008) Quorum quenching activity in Anabaena sp. PCC 7120: identification of AiiC, a novel AHL-acylase. FEMS Microbiol Lett 280:73–80. CrossRefPubMedGoogle Scholar
  93. Rutherford ST, Bassler BL (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2:a012427. CrossRefPubMedCentralPubMedGoogle Scholar
  94. Safari M, Amache R, Esmaeilishirazifard E, Keshavarz T (2014) Microbial metabolism of quorum-sensing molecules acyl-homoserine lactones, γ-heptalactone and other lactones. Appl Microbiol Biotechnol 98:3401–3412. CrossRefPubMedGoogle Scholar
  95. Scott RA, Lindow SE (2016) Transcriptional control of quorum sensing and associated metabolic interactions in Pseudomonas syringae strain B728a. Mol Microbiol 99:1080–1098. CrossRefPubMedGoogle Scholar
  96. Shepherd RW, Lindow SE (2009) Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology. Appl Environ Microbiol 75:45–53. CrossRefPubMedGoogle Scholar
  97. Singh RP, Desouky SE, Nakayama J (2016) Quorum quenching strategy targeting gram-positive pathogenic bacteria. Adv Microbiol Infect Dis Pub Health 2:109–130. CrossRefGoogle Scholar
  98. Stoltz DA, Meyerholz DK, Welsh MJ (2015) Origins of cystic fibrosis lung disease. N Engl J Med 372:351–362. CrossRefPubMedCentralPubMedGoogle Scholar
  99. Sun K, Liu J, Gao Y, Jin L, Gu Y, Wang W (2014) Isolation, plant colonization potential, and phenanthrene degradation performance of the endophytic bacterium Pseudomonas sp. Ph6-gfp. Sci Rep 4:5462. CrossRefPubMedCentralPubMedGoogle Scholar
  100. Teixeira N, Varahan S, Gorman MJ, Palmer KL, Zaidman-Remy A, Yokohata R, Nakayama J, Hancock LE, Jacinto A, Gilmore MS, Lopes MDFS (2013) Drosophila host model reveals new Enterococcus faecalis quorum-sensing associated virulence factors. PLoS One 8:e64740. CrossRefPubMedCentralPubMedGoogle Scholar
  101. Tichy EM, Luisi BF, Salmond GPC (2014) Crystal structure of the carbapenem intrinsic resistance protein CarG. J Mol Biol 426:1958–1970. CrossRefPubMedCentralPubMedGoogle Scholar
  102. Uroz S, Chhabra SR, Camara M, Williams P, Oger P, Dessaux Y (2005) N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151:3313–3322. CrossRefPubMedGoogle Scholar
  103. Uroz S, Oger PM, Chapelle E, Adeline MT, Faure D, Dessaux Y (2008) A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl Environ Microbiol 74:1357–1366. CrossRefPubMedCentralPubMedGoogle Scholar
  104. Uroz S, Dessaux Y, Oger P (2009) Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chembiochem 10:205–216. CrossRefPubMedGoogle Scholar
  105. Utari PD, Vogel J, Quax WJ (2017) Deciphering physiological functions of AHL quorum quenching acylases. Front Microbiol 8:1123. CrossRefPubMedCentralPubMedGoogle Scholar
  106. Valente R, Xavier K (2015) The Trk potassium transporter is required for RsmB-mediated activation of virulence in the phytopathogen pectobacterium wasabiae. J Bacteriol 198(2):248–255. CrossRefPubMedPubMedCentralGoogle Scholar
  107. Valente RS, Nadal-Jimenez P, Carvalho AF, Vieira FJ, Xavier KB (2017) Signal integration in quorum sensing enables cross-species induction of virulence in Pectobacterium wasabiae. MBio 8:e00398-17. CrossRefPubMedCentralPubMedGoogle Scholar
  108. Vasavi HS, Arun AB, Rekha PD (2016) Anti-quorum sensing activity of flavonoid-rich fraction from Centella asiatica L. against Pseudomonas aeruginosa PAO1. J Microbiol Immunol Infect 49:8–15. CrossRefPubMedGoogle Scholar
  109. von Bodman SB, Baue WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482. CrossRefGoogle Scholar
  110. Wang WZ, Morohoshi T, Ikenoya M, Someya N, Ikeda T (2010) AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium Microbacterium testaceum. Appl Environ Microbiol 76:2524–2530. CrossRefPubMedCentralPubMedGoogle Scholar
  111. Wang C, Yan C, Fuqua C, Zhang LH (2014) Identification and characterization of a second quorum-sensing system in Agrobacterium tumefaciens A6. J Bacteriol 196:1403–1411. CrossRefPubMedCentralPubMedGoogle Scholar
  112. Wang C, Yan C, Gao YG, Zhang LH (2015) D101 is critical for the function of AttJ, a repressor of quorum quenching system in Agrobacterium tumefaciens. J Microbiol 53:623–632. CrossRefPubMedGoogle Scholar
  113. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. CrossRefPubMedGoogle Scholar
  114. Wolf D, Rippa V, Mobarec JC, Sauer P, Adlung L, Kolb P, Bischofs IB (2015) The quorum-sensing regulator ComA from Bacillus subtilis activates transcription using topologically distinct DNA motifs. Nucleic Acids Res 44:2160–2172. CrossRefPubMedCentralPubMedGoogle Scholar
  115. Xue B, Chow JY, Baldansuren A, Yap LL, Gan YH, Dikanov SA, Robinson RC, Yew WS (2013) Structural evidence of a productive active site architecture for an evolved quorum-quenching GKL lactonase. Biochemistry 52:2359–2370. CrossRefPubMedCentralPubMedGoogle Scholar
  116. Yu X, Lund SP, Greenwald JW, Records AH, Scott RA, Nettleton D, Lindow SE, Gross DC, Beattie GA (2014) Transcriptional analysis of the global regulatory networks active in Pseudomonas syringae during leaf colonization. MBio 5:e01683-14. CrossRefPubMedCentralPubMedGoogle Scholar
  117. Zhang LH, Dong YH (2004) Quorum sensing and signal interference: diverse implications. Mol Microbiol 53:1563–1571. CrossRefPubMedGoogle Scholar
  118. Zhang S, Su H, Ma G, Liu Y (2016) Quantum mechanics and molecular mechanics study of the reaction mechanism of quorum quenching enzyme: N-acyl homoserine lactonase with C6-HSL. RSC Adv 6:23396–23402. CrossRefGoogle Scholar
  119. Zhou L, Zhang LH, Cámara M, He YW (2017) The DSF family of quorum sensing signals: diversity, biosynthesis, and turnover. Trends Microbiol 25:293–303. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Ashtaad Vesuna
    • 1
  • Anuradha S. Nerurkar
    • 1
  1. 1.Department of Microbiology and Biotechnology Centre, Faculty of ScienceThe Maharaja Sayajirao University of BarodaVadodaraIndia

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