Abstract
Pseudomonas aeruginosa is one of the vulnerable opportunistic pathogens associated with nosocomial infections, cystic fibrosis, burn wounds and surgical site infections. Several studies have reported that quorum sensing (QS) systems are controlled the P. aeruginosa pathogenicity. Hence, the targeting of QS considered as an alternative approach to control P. aeruginosa infections. This study aimed to evaluate the anti-quorum sensing and antibiofilm inhibitory potential of Musa paradisiaca against Chromobacterium violaceum (ATCC 12472) and Pseudomonas aeruginosa. The methanol extract of M. paradisiacsa exhibits that better antibiofilm potential against P. aeruginosa. Then, the crude methanol extract was subjected to purify by column chromatography and collected the fractions. The mass-spectrometric analysis of a methanol extract of M. paradisiaca revealed that 1,8-cineole is the major compounds. 1, 8-cineole significantly inhibited the QS regulated violacein production in C. violaceum. Moreover, 1,8-cineole significantly inhibited the QS mediated virulence production and biofilm formation of P. aeruginosa without affecting their growth. The real-time PCR analysis showed the downregulation of autoinducer synthase and transcriptional regulator genes upon 1,8-cineole treatment. The findings of the present study strongly suggested that metabolite of M. paradisiaca impedes P. aeruginosa QS system and associated virulence productions.
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Annapoorani A, Kalpana B, Musthafa KS, Pandian SK, Ravi AV (2013) Antipathogenic potential of Rhizophora spp. against the quorum sensing mediated virulence factors production in drug resistant Pseudomonas aeruginosa. Phytomedicine 20:956–963
Bjarnsholt T, Jensen PØ, Burmølle M, Hentzer M, Haagensen JA, Hougen HP, Høiby N (2005) Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151:373–383
Boyd A, Chakrabarty AM (1995) Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J Ind Microbiol 15:162–168
Cole SJ, Records AR, Orr MW, Linden SB, Lee VT (2014) Catheter-associated urinary tract infection by Pseudomonas aeruginosa is mediated by exopolysaccharide-independent biofilms. Infect Immun 82:2048–2058
Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036
Essar DW, Eberly LEE, Hadero A, 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
García-Contreras R (2016) Is quorum sensing interference a viable alternative to treat Pseudomonas aeruginosa infections? Front Microbiol 7:1454
Givskov M (2012) Beyond nutrition: health-promoting foods by quorum-sensing inhibition. Future Microbiol 7:1025–1028
Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574
Hall S, McDermott C, Anoopkumar-Dukie S, McFarland AJ, Forbes A, Perkins AV, Grant GD (2016) Cellular effects of pyocyanin, a secreted virulence factor of Pseudomonas aeruginosa. Toxins 8:236
Husain FM, Ahmad I, Al-thubiani AS, Abulreesh HH, AlHazza IM, Aqil F (2017) Leaf extracts of Mangifera indica L. Inhibit quorum sensing-regulated production of virulence factors and biofilm in test bacteria. Front Microbiol 8:727
Imam MZ, Akter S (2011) Musa paradisiaca L. and Musa sapientum L.: a phytochemical and pharmacological review. J Appl Pharm Sci 1:14–20
Kannappan A, Sivaranjani M, Srinivasan R, Rathna J, Pandian SK, Ravi AV (2017) Inhibitory efficacy of geraniol on biofilm formation and development of adaptive resistance in Staphylococcus epidermidis RP62A. J Med Microbiol 66:1506–1515
Karatuna O, Yagci AY (2010) Analysis of quorum sensing-dependent virulence factor production and its relationship with antimicrobial susceptibility in Pseudomonas aeruginosa respiratory isolates. Clin Microbiol Infect 16:1770–1775
Karuppiah V, Thiruganasambandam R (2017) Antibiofilm and quorum sensing inhibitory potential of Excoecaria agallocha against Pseudomonas aeruginosa. Int J Sci Invent Today 6:758–771
Karuppiah V, Thiruganasambandam R (2018) Anti-biofilm and quorum sensing inhibitory potential of Acanthus ilicifolius against uropathogens. Int J Life Sci 7:65–74
Karuppiah V, Thirunanasambandham R (2020) Quebrachitol from Rhizophora mucronata inhibits biofilm formation and virulence production in Staphylococcus epidermidis by impairment of initial attachment and intercellular adhesion. Arch Microbiol 202:1327–1340
Kessler E, Safrin M, Olson JC, Ohman DE (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268:7503–7508
Kessler E, Safrin M, Gustin JK, Ohman DE (1998) Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides. J Biol Chem 273:30225–30231
Koh CL, Sam CK, Yin WF, Tan LY, Krishnan T, Chong YM, Chan KG (2013) Plant-derived natural products as sources of anti-quorum sensing compounds. Sensors 13:6217–6228
Krasowska A, Sigler K (2014) How microorganisms use hydrophobicity and what does this mean for human needs? Front Cell Infect Microbiol 4:112
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
Lu L, Hume ME, Pillai SD (2005) Autoinducer-2-like activity on vegetable produce and its potential involvement in bacterial biofilm formation on tomatoes. Foodborne Pathog Dis 2:242–249
Luo J, Dong B, Wang K, Cai S, Liu T, Cheng X, Chen Y (2017) Baicalin inhibits biofilm formation, attenuates the quorum sensing-controlled virulence and enhances Pseudomonas aeruginosa clearance in a mouse peritoneal implant infection model. PLoS ONE 12:e0176883
Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O’toole GA (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310
Maura D, Hazan R, Kitao T, Ballok AE, Rahme LG (2016) Evidence for direct control of virulence and defense gene circuits by the Pseudomonas aeruginosa quorum sensing regulator, MvfR. Sci Rep 6:1–14
Merghni A, Noumi E, Hadded O, Dridi N, Panwar H, Ceylan O, Snoussi M (2018) Assessment of the antibiofilm and antiquorum sensing activities of Eucalyptus globulus essential oil and its main component 1,8-cineole against methicillin-resistant Staphylococcus aureus strains. Microb Pathog 118:74–80
Owlia P, Rasooli I, Saderi H, Aliahmadi M (2007) Retardation of biofilm formation with reduced productivity of alginate as a result of Pseudomonas aeruginosa exposure to Matricaria chamomilla essential oil. Pharmacogn Mag 3:83
Packiavathy IA, Priya S, Pandian SK, Ravi AV (2014) Inhibition of biofilm development of uropathogens by curcumin–an anti-quorum sensing agent from Curcuma longa. Food Chem 148:453–460
Parasuraman P, Devadatha B, Sarma VV, Ranganathan S, Ampasala DR, Siddhardha B (2020) Anti-quorum sensing and antibiofilm activities of Blastobotrys parvus PPR3 against Pseudomonas aeruginosa PAO1. Microb Pathog 138:103811
Pereira A, Maraschin M (2015) Banana (Musa spp) from peel to pulp: ethnopharmacology, source of bioactive compounds and its relevance for human health. J Ethnopharmacol 160:149–163
Santhakumari S, Kannappan A, Pandian SK, Thajuddin N, Rajendran RB, Ravi AV (2016) Inhibitory effect of marine cyanobacterial extract on biofilm formation and virulence factor production of bacterial pathogens causing vibriosis in aquaculture. J Appl Phycol 28:313–324
Sethupathy S, Nithya C, Pandian SK (2015) 2-Furaldehyde diethyl acetal from tender coconut water (Cocos nucifera) attenuates biofilm formation and quorum sensing-mediated virulence of Chromobacterium violaceum and Pseudomonas aeruginosa. Biofouling 31:721–733
Sivaranjani M, Srinivasan R, Aravindraja C, Karutha Pandian S, Veera Ravi A (2018) Inhibitory effect of α-mangostin on Acinetobacter baumannii biofilms: an in vitro study. Biofouling 34:579–593
Soni KA, Lu L, Jesudhasan PR, Hume ME, Pillai SD (2008) Influence of autoinducer-2 (AI-2) beef sample extracts on E. coli O157:H7 survival and gene expression of virulence genes yadK and hhA. J Food Sci 73:M135-139
Stapper AP, Narasimhan G, Ohman DE, Barakat J, Hentzer M, Molin S, Mathee K (2004) Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J Med Microbiol 53:679–690
Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, Stevigny C, Duez P, Rajaonson S, El Jaziri M (2011) The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Microbiology 157:2120–2132
Vasavi HS, Arun AB, Rekha PD (2013) Inhibition of quorum sensing in Chromobacterium violaceum by Syzygium cumini L. and Pimenta dioica L. Asian Pac J Trop Biomed 3:954–959
Vijayakumar K, Ramanathan T (2018) Antiquorum sensing and biofilm potential of 5-hydroxymethylfurfural against Gram positive pathogens. Microb Pathog 125:48–50
Vijayakumar K, Ramanathan T (2020) Musa acuminata and its bioactive metabolite 5-hydroxymethylfurfural mitigates quorum sensing (las and rhl) mediated biofilm and virulence production of nosocomial pathogen Pseudomonas aeruginosa in vitro. J Ethnopharmacol 246:112242
Vijayakumar K, Bharathidasan V, Manigandan V, Jeyapragash D (2020) Quebrachitol inhibits biofilm formation and virulence production against methicillin-resistant Staphylococcus aureus. Microb Pathog 149:104286
Wang S, Yu S, Zhang Z, Wei Q, Yan L, Ai G, Ma LZ (2014) Coordination of swarming motility, biosurfactant synthesis, and biofilm matrix exopolysaccharide production in Pseudomonas aeruginosa. Appl Environ Microbiol 80:6724–6732
Wu DC, Chan WW, Metelitsa AI, Fiorillo L, Lin AN (2011) Pseudomonas skin infection. Am J Clin Dermatol 12:157–169
Yu Y, Cheng AS, Wang L, Dunne WM, Bayliss SJ (2007) Hot tub folliculitis or hot hand–foot syndrome caused by Pseudomonas aeruginosa. J Am Acad Dermatol 57:596–600
Zhu H, He CC, Chu QH (2011) Inhibition of quorum sensing in Chromobacterium violaceum by pigments extracted from Auricularia auricular. Lett Appl Microbiol 52:269–274
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The authors gratefully thank Dr. G. Ashwinkumar Subramenium for support in discussing and fulfilling the work. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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VK Conceptualization of whole work, performed the experiments, data analyzed and co-wrote the manuscript. RT, GT; Performed the experiments, data analyzed and co-wrote the manuscript.
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Karuppiah, V., Thirunanasambandham, R. & Thangaraj, G. Anti-quorum sensing and antibiofilm potential of 1,8-cineole derived from Musa paradisiaca against Pseudomonas aeruginosa strain PAO1. World J Microbiol Biotechnol 37, 66 (2021). https://doi.org/10.1007/s11274-021-03029-y
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DOI: https://doi.org/10.1007/s11274-021-03029-y