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
› Institutsangaben
Weitere Informationen

Publikationsverlauf

received 24. Oktober 2013
revised 07. Januar 2014

accepted 09. Januar 2014

Publikationsdatum:
31. Januar 2014 (online)

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.

 
  • References

  • 1 Donlan RM, Costerton JW. Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-193
  • 2 Davey ME, OʼToole GA. Microbial biofilms: From ecology to molecular genetics. Microbiol Mol Biol Rev 2000; 64: 847-867
  • 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
  • 4 Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilm: From the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2: 95-108
  • 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
  • 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
  • 7 Mukherjee PK, Chandra J. Candida biofilm resistance. Drug Resist Updat 2004; 7: 301-309
  • 8 Gilbert P, Das J, Foley I. Biofilm susceptibility to antimicrobials. Adv Dent Res 1997; 11: 160-167
  • 9 Shiner EK, Rumbaugh P, Williams SC. Interkingdom signaling: Deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 2005; 29: 935-947
  • 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
  • 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
  • 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
  • 13 Choo JH, Rukayadi Y, Hwang JK. Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 2006; 42: 637-641
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 24 Quave CL, Plano LRW, Bennett BC. Quorum Sensing Inhibitors of Staphylococcus aureus from Italian Medicinal Plants. Planta Med 2011; 77: 188-195
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 31 Chowdhury R, Hasan MC, Rashid MA. Antimicrobial activity of Toona ciliata and Amoora rohituka . Fitoterapia 2003; 74: 155-158
  • 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
  • 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
  • 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
  • 35 Nagalakshmi MAH, Thangadurai D, Muralidara Rao D, Pullaiah T. Phytochemical and antimicrobial study of Chukrasia tabularis leaves. Fitoterapia 2001; 72: 62-64
  • 36 Sahgal G. In vitro and in vivo anticandidal activity of Swietenia mahogani methanolic seed extract. Trop Biomed 2011; 28: 132-137
  • 37 Cella M, Riva DA, Coulombie FC, Mersich SE. Virucidal activity presence in Trichilia glabra leaves. Rev Argent Microbiol 2004; 36: 136-138
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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
  • 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