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Planta Med 2014; 80(04): 343-350
DOI: 10.1055/s-0033-1360337
Biological Screening
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Inhibition of Bacterial Quorum Sensing and Biofilm Formation by Extracts of Neotropical Rainforest Plants

Chieu Anh Ta
1   Laboratory for Analysis of Natural and Synthetic Environmental Toxins (LANSET), Department of Biology, University of Ottawa, Ottawa, Canada
,
Marie Freundorfer
1   Laboratory for Analysis of Natural and Synthetic Environmental Toxins (LANSET), Department of Biology, University of Ottawa, Ottawa, Canada
,
Thien-Fah Mah
2   Department of Biochemistry, Microbiology and Immunology, University of Ottawa, Ottawa, Canada
,
Marco Otárola-Rojas
3   Herbario Juvenal Valerio Rodriguez, Universidad Nacional, Heredia, Costa Rica
,
Mario Garcia
3   Herbario Juvenal Valerio Rodriguez, Universidad Nacional, Heredia, Costa Rica
,
Pablo Sanchez-Vindas
3   Herbario Juvenal Valerio Rodriguez, Universidad Nacional, Heredia, Costa Rica
,
Luis Poveda
3   Herbario Juvenal Valerio Rodriguez, Universidad Nacional, Heredia, Costa Rica
,
J. Alan Maschek
4   Department of Chemistry, University of South Florida, Tampa, FL, United States
,
Bill J. Baker
4   Department of Chemistry, University of South Florida, Tampa, FL, United States
,
Allison L. Adonizio
5   Center for Ethnobiology and Natural Products (CENaP), Department of Biological Sciences, Florida International University, Miami, FL, United States
,
Kelsey Downum
5   Center for Ethnobiology and Natural Products (CENaP), Department of Biological Sciences, Florida International University, Miami, FL, United States
,
Tony Durst
6   Department of Chemistry, University of Ottawa, Ottawa, Canada
,
John T. Arnason
1   Laboratory for Analysis of Natural and Synthetic Environmental Toxins (LANSET), Department of Biology, University of Ottawa, Ottawa, Canada
› Author Affiliations
Further Information

Publication History

received 24 October 2013
revised 07 January 2014

accepted 09 January 2014

Publication Date:
31 January 2014 (online)

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Abstract

Bacterial biofilms are responsible for many persistent infections by many clinically relevant pathogens such as Staphylococcus aureus and Pseudomonas aeruginosa. Biofilms are much more resistant to conventional antibiotics than their planktonic counterparts. Quorum sensing, an intercellular communication system, controls pathogenesis and biofilm formation in most bacterial species. Quorum sensing provides an important pharmacological target since its inhibition does not provide a selective pressure for resistance. In this study, we investigated the quorum sensing and biofilm inhibitory activities of 126 plant extracts from 71 species collected from neotropical rainforests in Costa Rica. Quorum sensing and biofilm interference were assessed using a modified disc diffusion bioassay with Chromobacterium violaceum ATCC 12 472 and a spectrophotometric bioassay with Pseudomonas aeruginosa PA14, respectively. Species with significant anti-quorum sensing and/or anti-biofilm activities belonged to the Meliaceae, Melastomataceae, Lepidobotryaceae, Sapindaceae, and Simaroubaceae families. IC50 values ranged from 45 to 266 µg/mL. Extracts of these active species could lead to future development of botanical treatments for biofilm-associated infections.

Key words

biofilms - quorum sensing - Meliaceae - Melastomataceae - Piperaceae - violacein - Chromobacterium violaceum - Pseudomonas aeruginosa
 

  • References

  • 1 Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-193
    CrossrefPubMedGoogle Scholar
  • 2 Davey ME, OʼToole GA. Microbial biofilms: From ecology to molecular genetics. Microbiol Mol Biol Rev 2000; 64: 847-867
    CrossrefPubMedGoogle Scholar
  • 3 Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 1998; 280: 295-298
    CrossrefPubMedGoogle Scholar
  • 4 Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilm: From the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2: 95-108
    CrossrefPubMedGoogle Scholar
  • 5 Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000; 407: 762-764
    CrossrefPubMedGoogle Scholar
  • 6 Kalmokoff M, Lanthier P, Tremblay T, Foss M, Lau PC, Sanders G, Austin J, Kelly J, Szymanski CM. Proteomic analysis of Campylobacter jejuni 11 168 biofilms reveals a role for the motility complex in biofilm formation. J Bacteriol 2006; 188: 4312-4320
    CrossrefPubMedGoogle Scholar
  • 7 Mukherjee PK, Chandra J. Candida biofilm resistance. Drug Resist Updat 2004; 7: 301-309
    CrossrefPubMedGoogle Scholar
  • 8 Gilbert P, Das J, Foley I. Biofilm susceptibility to antimicrobials. Adv Dent Res 1997; 11: 160-167
    CrossrefPubMedGoogle Scholar
  • 9 Shiner EK, Rumbaugh P, Williams SC. Interkingdom signaling: Deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 2005; 29: 935-947
    CrossrefPubMedGoogle Scholar
  • 10 Givskov M, de Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD, Kjellelberg S. Eukaryotic interference with homoserine lactone-mediated prokaryotic signaling. J Bacteriol 1996; 178: 6618-6622
    PubMedGoogle Scholar
  • 11 Raffa RB, Iannuzzo JR, Levine DR, Saeid KK, Schwartz RC, Sucic NT, Terleckyj OD, Young JM. Bacterial communication (“quorum sensing”) via ligands and receptors: A novel pharmacologic target for the design of antibiotic drugs. J Pharmacol Exp Ther 2005; 312: 417-423
    PubMedGoogle Scholar
  • 12 Teplitski M, Robinson JB, Bauer WD. Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 2000; 13: 637-648
    CrossrefPubMedGoogle Scholar
  • 13 Choo JH, Rukayadi Y, Hwang JK. Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 2006; 42: 637-641
    PubMedGoogle Scholar
  • 14 Girennavar B, Cepeda ML, Soni KA, Vikram A, Jesudhasan P, Jayaprakasha GK, Pillai SD, Patil BS. Grapefruit juice and its furocoumarins inhibits autoinducer signaling and biofilm formation in bacteria. Int J Food Microbiol 2008; 125: 204-208
    CrossrefPubMedGoogle Scholar
  • 15 Bjarnsholt T, Jensen PO, Rasmussen TB, Chrisphersen L, Calum H, Hentzer M, Hougen H, Rygaard J, Moser C, Eberl L, Hoiby N, Givskov M. Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 2005; 151: 3873-3880
    CrossrefPubMedGoogle Scholar
  • 16 Quave CL, Estévez-Carmona M, Compadre CM, Hobby G, Hendrickson H, Beenken KE, Smeltzer MS. Ellagic acid derivatives from Rubus ulmifolius inhibit Staphylococcus aureus biofilm formation and improve response to antibiotics. PLos One 2012; 7: e28737
    CrossrefPubMedGoogle Scholar
  • 17 Adonizio A. Anti-quorum sensing agents from south Florida medicinal plants and their attenuation of Pseudomonas aeruginosa pathogenicity [dissertation]. Miami: Florida International University; 2008
    PubMedGoogle Scholar
  • 18 Riedel K, Boustie J, Eberl L, Berg G, Grube M. Effects of lichen secondary metabolites on bacterial functions and biofilm formation. Planta Med 2008; 74: PA85
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Ren D, Zuo R, Barrios AFG, Bedzyk LA, Eldridge GR, Pasmore ME, Wood TK. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl Environ Microbiol 2005; 71: 4022-4034
    CrossrefPubMedGoogle Scholar
  • 20 Cartagena E, Colom OA, Neske A, Valdez JC, Bardón A. Effects of plant lactones on the production of biofilm of Pseudomonas aeruginosa . Chem Pharm Bull 2007; 55: 22-25
    CrossrefPubMedGoogle Scholar
  • 21 Kuźma L, Rózalski M, Walencka E, Rózalska B, Wysokińska H. Antimicrobial activity of diterpenoids from hairy roots of Salvia sclarea L.: Salvipisone as a potential anti-biofilm agent active against antibiotic resistant staphylococci. Phytomedicine 2007; 14: 31-35
    PubMedGoogle Scholar
  • 22 Adonizio AL, Downum K, Bennett BC, Mathee K. Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 2006; 105: 427-435
    CrossrefPubMedGoogle Scholar
  • 23 Adonizio A, Kong KF, Mathee K. Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob Agents Chemother 2008; 52: 198-203
    CrossrefPubMedGoogle Scholar
  • 24 Quave CL, Plano LRW, Bennett BC. Quorum Sensing Inhibitors of Staphylococcus aureus from Italian Medicinal Plants. Planta Med 2011; 77: 188-195
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 Cech NB, Junio HA, Ackermann LW, Kavanaugh JS, Horswill AR. Quorum quenching and antimicrobial activity of goldenseal (Hydrastis canadensis) against methicillin-resistant Staphylococcus aureus (MRSA). Planta Med 2012; 78: 1556-1561
    Article in Thieme ConnectPubMedGoogle Scholar
  • 26 McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GS, Williams P. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 1997; 143: 3703-3711
    CrossrefPubMedGoogle Scholar
  • 27 Omar S, Zhang J, Mackinnon S, Leaman D, Durst T, Philogene BJR, Arnason JT, Sanchez-Vindas PE, Poveda L, Tamez PA, Pezzuto JM. Traditionally-used antimalarials from the Meliaceae. Curr Top Med Chem 2003; 3: 137-139
    PubMedGoogle Scholar
  • 28 Zhang Y, Wang JS, Wang XB, Gu YC, Wei DD, Guo C, Yang MH, Kong LY. Limonoids from the fruits of Aphanamixis polystachya (Meliaceae) and their biological activities. J Agric Food Chem 2013; 61: 2171-2182
    CrossrefPubMedGoogle Scholar
  • 29 Miranda Júnior RN, Dolabela MF, da Silva MN, Póvoa MM, Maia JG. Antiplasmodial activity of the andiroba (Carapa guianensis Aubl., Meliaceae) oil and its limonoid-rich fraction. J Ethnopharmacol 2012; 142: 679-683
    CrossrefPubMedGoogle Scholar
  • 30 Kvist LP, Christensen SB, Rasmussen HB, Mejia K, Gonzalez A. Identification and evaluation of Peruvian plants used to treat malaria and leishmaniasis. J Ethnopharmacol 2006; 106: 390-402
    CrossrefPubMedGoogle Scholar
  • 31 Chowdhury R, Hasan MC, Rashid MA. Antimicrobial activity of Toona ciliata and Amoora rohituka . Fitoterapia 2003; 74: 155-158
    CrossrefPubMedGoogle Scholar
  • 32 Govindachari TR, Suresh G, Banumathy B, Masimalani S, Gopalakrishnan G, Krishna Kumari GN. Antifungal activity of some B,D-secolimonoids from two meliaceous plants. J Chem Ecol 1993; 25: 923-933
    PubMedGoogle Scholar
  • 33 Kanwal Q, Hussain I, Siddiqui HL, Javaid A. Antimicrobial activity screening of isolated flavonoids from Azadirachta indica leaves. J Serb Chem Soc 2011; 76: 375-384
    CrossrefPubMedGoogle Scholar
  • 34 Malairajan P, Narasimhan S, Gopalakrishnan G, Veni KJK. Semisynthetic modification of cedrelone and its antimicrobial activity. Int J Drug Dev Res 2012; 4: 385-392
    PubMedGoogle Scholar
  • 35 Nagalakshmi MAH, Thangadurai D, Muralidara Rao D, Pullaiah T. Phytochemical and antimicrobial study of Chukrasia tabularis leaves. Fitoterapia 2001; 72: 62-64
    CrossrefPubMedGoogle Scholar
  • 36 Sahgal G. In vitro and in vivo anticandidal activity of Swietenia mahogani methanolic seed extract. Trop Biomed 2011; 28: 132-137
    PubMedGoogle Scholar
  • 37 Cella M, Riva DA, Coulombie FC, Mersich SE. Virucidal activity presence in Trichilia glabra leaves. Rev Argent Microbiol 2004; 36: 136-138
    PubMedGoogle Scholar
  • 38 Chung KT, Stevens jr. SE, Lin WF, Wei CI. Growth inhibition of selected food-borne bacteria by tannic acid, propyl gallate and related compounds. Lett Appl Microbiol 1993; 17: 29-32
    CrossrefPubMedGoogle Scholar
  • 39 Pai MR, Acharya LD, Udupa N. Evaluation of antiplaque activity of Azadirachta indica leaf extract gel – a 6-week clinical study. J Ethnopharmacol 2004; 90: 99-103
    CrossrefPubMedGoogle Scholar
  • 40 Chaturvedula VSP, Gao Z, Jones SH, Feng X, Hecht SM, Kingston DGI. A new ursane triterpene from Monochaetum vulcanicum that inhibits DNA polymerase β lyase. J Nat Prod 2004; 67: 899-901
    CrossrefPubMedGoogle Scholar
  • 41 Setzer WN, Vogler B, Schmidt JM, Petty JL, Haber WA. Isolation of cupanioside, a novel cytotoxic and antibacterial long-chain fatty alcohol glycoside from the bark of Cupania glabra . Planta Med 2005; 71: 686-688
    Article in Thieme ConnectPubMedGoogle Scholar
  • 42 Franssen FF, Smeijsters LJ, Berger I, Medinilla Aldana BE. In vivo and in vitro antiplasmodial activities of some plants traditionally used in Guatemala against malaria. Antimicrob Agents Chemother 1997; 41: 1500-1503
    PubMedGoogle Scholar
  • 43 OʼNeill MJ, Bray DH, Boardman P, Wright CW, Phillipson JD, Warhurst DC, Gupta MP, Correya M, Solis P. Plants as sources of antimalarial drugs, part 6: Activities of Simarouba amara fruits. J Ethnopharmacol 1988; 22: 183-190
    CrossrefPubMedGoogle Scholar
  • 44 Caceres A, Cano O, Samayoa B, Aguilar L. Plants used in Guatemala for the treatment of gastrointestinal disorders. 1. Screening of 84 plants against enterobacteria. J Ethnopharmacol 1990; 30: 55-73
    CrossrefPubMedGoogle Scholar
  • 45 Omar S, Marcotte M, Fields P, Sanchez PE, Poveda L, Mata R, Jimenez A, Durst T, Zhang J, MacKinnon S, Leaman D, Arnason JT, Philogene BJR. Antifeedant activities of terpenoids isolated from tropical Rutales. J Stored Prod Res 2007; 43: 92-96
    CrossrefPubMedGoogle Scholar