Abstract
Quorum sensing (QS) plays an important role in virulence, biofilm formation and survival of many pathogenic bacteria including Pseudomonas aeruginosa. This signalling pathway is considered as novel and promising target for anti-infective agents. In the present investigation, effect of the Sub-MICs of clove oil on QS regulated virulence factors and biofilm formation was evaluated against P. aeruginosa PAO1 and Aeromonas hydrophila WAF-38 strain. Sub-inhibitory concentrations of the clove oil demonstrated statistically significant reduction of las- and rhl-regulated virulence factors such as LasB, total protease, chitinase and pyocyanin production, swimming motility and exopolysaccharide production. The biofilm forming capability of PAO1 and A. hydrophila WAF-38 was also reduced in a concentration-dependent manner at all tested sub-MIC values. Further, the PAO1-preinfected Caenorhabditis elegans displayed an enhanced survival when treated with 1.6% v/v of clove oil. The above findings highlight the promising anti-QS-dependent therapeutic function of clove oil against P. aeruginosa.
Similar content being viewed by others
References
Adonizio AL, Downum K, Bennett BC and Mathee K 2006 Anti-quorum sensing activity of medicinal plants in southern Florida. J. Ethnopharmacol. 103 427–435
Adonizio AL, Kong KF and Mathee K 2008a Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob. Agents Chemother. 52 198–203
Adonizio A, Leal SM, Ausubel FM and Mathee K 2008b Attenuation of Pseudomonas aeruginosa virulence by medicinal plants in a Caenorhabditis elegans model system. J. Med. Microbiol. 57 809–813
Ahmad I, Aqil F, Ahmad F, Zahin M and Musarrat J 2008 Quorum sensing in bacteria: potential in plant health protection; in Plant–bacteria interactions (eds) I Ahmad, S Hayat and J Pichtel (Weinheim, Germany: Wiley) pp129–153
Bala A, Kumar R, Harjai K 2011 Inhibition of quorum sensing in Pseudomonas aeruginosa by azithromycin and its effectiveness in urinary tract infections. J. Med. Microbiol. 60 300–306
Clinical and Laboratory Standards Institute 2007 Performance standards for antimicrobial susceptibility testing: Seventeenth informational supplement: M100-S17. CLSI, Wayne, PA, USA
Dubois MK, Gils JK, Hanniton PA and Smith F 1956 Use of phenol reagent for the determination of total sugar. Anal. Chem. 28 350–356
Essar DW, Eberly L, Hadero A and Crawford IP 1990 Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J. Bacteriol. 172 884–900
Fuqua C, Parsek MR and Greenberg EP 2001 Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Ann. Rev. Genet. 35 439–468
Gallagher LA and Manoil C 2001 Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J. Bacteriol. 183 6207–6214
Harjai K, Kumar R and Singh S 2010 Garlic blocks quorum sensing and attenuates the virulence of Pseudomonas aeruginosa. FEMS Immun. Med. Microbiol. 58 161–168
Hentzer M and Givskov M 2003 Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Investig. 112 1300–1307
Hentzer M, Reidel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Hoiby N, Kjelleberg S and Givskov M 2002 Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiol. 148 87–102
Huerta V, Mihalik K, Crixell SH and Vattem DA 2008 Herbs, spices and medicinal plants used in hispanic traditional medicine can decrease quorum sensing dependent virulence in Pseudomonas aeruginosa. Int. J. Appl. Res. Nat. Prod. 1 9–15
Husain FM and Ahmad I 2013 Doxycycline interferes with quorum sensing-mediated virulence factors and biofilm formation in Gram-negative bacteria. World J. Microbiol. Biotechnol. 29 949–957
Huston AL, Methe B and Deming JW 2004 Purification, characterization and sequencing of an extracellular cold-active aminopeptidase produced by marine psychrophile Colwellia psychrerythraea strain 34H. Appl. Environ. Microbiol. 70 3321–3328
Jaramillo-Colorado B, Olivero-Verbel J, Stashenko EE, Wagner-Döbler I and Kunze B 2012 Anti-quorum sensing activity of essential oils from Colombian plants. Nat. Prod. Res. 26 1075–1086
Kalia VC 2013 Quorum sensing inhibitors: An overview. Biotechnol. Adv. 31 224–245
Kavanaugh NL and Ribbeck K 2012 Selected antimicrobial essential oils eradicate Pseudomonas spp. and Staphylococcus aureus biofilms. Appl. Environ. Microbiol. 78 4057–4061
Kessler E, Safrin M, Olson JC and Ohman DE 1993 Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J. Biol. Chem. 268 7503–7508
Khajanchi BK, Fadl AA, Borchardt MA, Berg RL, Horneman AJ, Stemper ME, Joseph SW, Moyer NP, Sha J and Chopra AK 2010 Distribution of virulence factors and molecular fingerprinting of Aeromonas species isolates from water and clinical samples: suggestive evidence of water-to-human transmission. Appl. Environ. Microbiol. 76 2313–2325
Khan MSA, Zahin M, Hasan S, Husain FM and Ahmad I 2009 Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett. Appl. Microbiol. 49 354–360
Kjelleberg S and Molin S 2002 Is there a role for quorum sensing signals in bacterial biofilms? Curr. Opin. Microbiol. 5 254–258
Lee J, Wu J, Deng Y, Wang J, Wang C, Wang J, Chang C, Dong Y, Williams P and Zhang LH 2013 A cell-cell communication signal integrates quorum sensing and stress response. Nat. Chem. Biol. 9 339–343
Lewis K 2007 Persister cells, dormancy and infectious disease. Nat. Rev. Microbiol. 5 48–56
Lynch MJ, Swift S, Kirke DF, Keevil CW, Dodd CER and Williams P 2002 The regulation of biofilm development by quorum sensing in Aeromonas hydrophila. Environ. Microbiol. 4 18–28
Moy TI, Ball AR, Anklesaria Z, Casadei G, Lewis K and Ausubel FM 2006 Identification of novel antimicrobials using a live-animal infection model. PNAS 103 10414–10419
Musthafa KS, Sivamurthy BS, Packiavathy ISV, Pandian SK, and Ravi AV 2012 Quorum sensing inhibition in Pseudomonas aeruginosa PAO1 by antagonistic compound phenylacetic acid. Curr. Microbiol. DOI 10.1007/s00284-012-0181-9
Musthafa KS, Ravi AV, Annapoorani A, Packiavathy ISV and Pandian SK 2010 Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of the N-acyl homoserine lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa. Chemotherapy 56 333–339
Nakamiya K, Hashimoto S, Ito H, Edmonds JS, Yasuhara A and Morita M 2005 Microbial treatment of bis (2-ethylhexyl) phthalate in polyvinyl chloride with isolated bacteria. J. Biosci. Bioeng. 99 115–9
O’Toole GA and Kolter R 1998 Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol. Microbiol. 28 449–461
Packiavathy IASV, Agilandeswari P, Musthafa KS, Pandian SK and Ravi AV 2012 Antibiofilm and quorum sensing inhibitory potential of Cuminum cyminum and its secondary metabolite methyl eugenol against gram negative bacterial pathogens. Food Res. Int. 45 85–92
Pearson JP, Gray KM, Passador L, Tucker KD, Eberhard A, Iglewski BH and Greenberg EP 1994 Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91 197–201
Pesci EC, Pearson JP, Seed PC and Iglewski BH 1997 Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179 3127–3132
Pessi G and Haas D 2000 Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J. Bacteriol. 182 6940–6949
Ponnusamy K, Paul D and Kweon JH 2009 Inhibition of quorum sensing mechanism and Aeromonas hydrophila biofilm formation by vanillin. Environ. Engg. Sci. 26 1359–1363
Rasmussen TB, Bjarnsholt T, Skindersoe ME, Hentzer M, Kristoffersen P, Köte M, Nielsen J, Eberl L and Givskov M 2005 Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J. Bacteriol. 187 1799–1814
Rasmussen TB and Givskov M 2006 Quorum-sensing inhibitors as antipathogenic drugs. Int. J. Med. Microbiol. 296 149–161
Rasmussen TB, Manefield M, Andersen JB, Eberl L, Anthoni U, Christophersen C, Steinberg P, Kjelleberg S and Givskov M 2000 How Delisea pulchra furanones affect quorum sensing and swarming motility in Serratia liquefaciens MG1. Microbiology 146 3237–3244
Rumbaugh KP 2004 The Language of Bacteria…and Just About Everything Else. The Scientist 18 26–27
Rumbaugh KP, Diggle SP, Watters SM, Ross-Gillespie A, Griffin AS and West SA 2009 Quorum sensing and the social evolution of bacterial virulence. Curr. Biol. 19 341–345
Rutherford ST and Bassler BL 2012 Bacterial quorum sensing: Its role in virulence and possibilities for its control. Cold Spring Harbor Perspec. Med. 2 a012427
Sameena H 2006 Quorum sensing inhibition and antimicrobial properties of certain medicinal plants and natural products, MSc Thesis, Aligarh Muslim University, Aligarh, India
Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB, Bjarnsholt T, Tolke-Nielsen T, Høiby N and Givskov M 2008 Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 52 648–3663
Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK Chhabra SR, Williams P, Macintyre S and Stewart GSAB 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
Swift S, Lynch MJ, Fish L, Kirke DF, Tomas JM, Stewart GSAB and Williams P 1999 Quorum sensing-dependent regulation and blockade of exoprotease production in Aeromonas hydrophila. Infect. Immun. 67 5192–5199
Szabo MA, Varga GZ, Hohmann J, Schelz Z and Szegedi E 2010 Inhibition of quorum-sensing signals by essential oils. Phytother. Res. 24 782–786
Tagannaa JC, Quanicoc JP, Peronoc RMG, Amorc EC and Riveraa WL 2011 Tannin-rich fraction from Terminalia catappa inhibits quorum sensing (QS) in Chromobacterium violaceum and the QS-controlled biofilm maturation and LasA staphylolytic activity in Pseudomonas aeruginosa. J. Ethnopharmcol. 134 865–871
Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, Stévigny C, Duez P, Rajaonson S, Diallo B, Mol A, Baucher M and El Jaziri M 2011 The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Microbiology 157 2120–2132
Vattem DA, Mihalik K, Crixell SH and McLean RJ 2007 Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78 302–310
Williams P 2007 Quorum sensing, communication and cross kingdom signalling in the bacterial world. Microbiology 153 3923–3928
Zahin M, Hasan S, Aqil F, Khan MSA, Husain FM and Ahmad I 2010 Screening of Indian medicinal plants for their anti-quorum sensing activity. Ind. J. Exp. Biol. 48 1219–1224
Zhang LH and Dong YH 2004 Quorum sensing and signal interference: diverse implications. Mol. Microbiol. 53 1563–1571
Zhou L, Zheng H, Tang Y, Yu W and Gong Q 2013 Eugenol inhibits quorum sensing at sub-inhibitory concentrations. Biotechnol. Lett. 35 631–637
Acknowledgements
The authors acknowledge the financial support provided by the University Grants Commission (Grant No. F. 33-208/2007) and the Department of Science and Technology (DST), New Delhi, India, for awarding the INSPIRE fellowship to FMH. We are also thankful to Prof Robert JC McLean (University of Texas, USA) and Prof Thomas K Wood (Pennsylvania State University, USA) for providing QS bioreporter strains. We are also grateful to Dr Ruchita Pal, AIRF, JNU, New Delhi, India, for her kind assistance in using the scanning electron microscope (SEM) facility.
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: DURGADAS P KASBEKAR
MS received 27 March 2013; accepted 16 September 2013
Corresponding editor: Durgadas P Kasbekar
[Husain FM, Ahmad I, Asif M and Tahseen Q 2013 Influence of clove oil on certain quorum-sensing-regulated functions and biofilm of Pseudomonas aeruginosa and Aeromonas hydrophila. J. Biosci. 38 1–10] DOI 10.1007/s12038-013-9385-9
Rights and permissions
About this article
Cite this article
Husain, F.M., Ahmad, I., Asif, M. et al. Influence of clove oil on certain quorum-sensing-regulated functions and biofilm of Pseudomonas aeruginosa and Aeromonas hydrophila . J Biosci 38, 835–844 (2013). https://doi.org/10.1007/s12038-013-9385-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-013-9385-9