Abstract
The focal intent of this study was to find out an alternative strategy for the antibiotic usage against bacterial infections. The quorum sensing inhibitory (QSI) activity of marine sponges collected from Palk Bay, India was evaluated against acyl homoserine lactone (AHL) mediated violacein production in Chromobacterium violaceum (ATCC 12472), CV026 and virulence gene expressions in clinical isolate Serratia marcescens PS1. Out of 29 marine sponges tested, the methanol extracts of Aphrocallistes bocagei (TS 8), Haliclona (Gellius) megastoma (TS 25) and Clathria atrasanguinea (TS 27) inhibited the AHL mediated violacein production in C. violaceum (ATCC 12472) and CV026. Further, these sponge extracts inhibited the AHL dependent prodigiosin pigment, virulence enzymes such as protease, hemolysin production and biofilm formation in S. marcescens PS1. However, these sponge extracts were not inhibitory to bacterial growth, which reveals the fact that the QSI activity of these extracts was not related to static or killing effects on bacteria. Based on the obtained results, it is envisaged that the marine sponges could pave the way to prevent quorum sensing (QS) mediated bacterial infections.
Similar content being viewed by others
References
Adonizio A, Kong KF, Mathee K (2008) Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by south florida plant extracts. Antimicrob Agents Chemother 52:98–203
Bhargava N, Sharma P, Capalash N (2010) Quorum sensing in Acinetobacter: an emerging pathogen. Crit Rev Microbiol 36:349–360
Borchardt SA, Allain EJ, Michels JJ, Stearns GW, Kelly RF, McCoy WF (2001) Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl Environ Microbiol 67:3174–3179
Choo JH, Rukayadi Y, Hwang JK (2006) Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 42:637–641
Harjai K, Kumar R, Sukhvinder S (2010) Garlic blocks quorum sensing and attenuates the virulence of Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 58:161–168
Hejazi A, Falkiner FR (1997) Serratia marcescens. J Med Microbiol 46:903–912
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
Kalia VC, Purohit HJ (2011) Quenching the quorum sensing system: potential antibacterial drug targets. Crit Rev Microbiol 37:121–140
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
Khadar SM, Shunmugiah KP, Arumugam VR (2012) Inhibition of quorum-sensing-dependent phenotypic expression in Serratia marcescens by marine sediment Bacillus spp. SS4. Ann Microbiol 62:443–447
Khan MSA, Zahin M, Hasan S, Husain FM, 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
Kim JS, Kim YH, Seo YW, Park S (2007) Quorum sensing inhibitors from the red alga, Ahnfeltiopsis flabelliformis. Biotechnol Bioprocess Eng 12:308–311
Kumar RJ, Zi-rong X (2004) Biomedical compounds from marine organisms. Mar Drugs 2:123–146
Manefield M, Rocky DN, Kumar N, Read R, Givskov M, Steinberg P, Kjelleberg S (1999) Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145:283–291
McLean RJC, Pierson LS, Fuqua C (2004) A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 58:351–360
Musthafa KS, Ravi AV, Annapoorani A, Packiavathy ISV, Pandian SK (2010) Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of N-acyl-homoserine-lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa. Chemotherapy 56:333–339
Musthafa KS, Saroja V, Pandian SK, Ravi AV (2011) Antipathogenic potential of marine Bacillus sp. SS4 on N-acyl-homoserine-lactone-mediated virulence factors production in Pseudomonas aeruginosa (PAO1). J Biosci 36:55–67
Narsinh LT, Werner EGM (2004) Biotechnological potential of marine sponges. Curr Sci 86:10-11
Nithya C, Aravindraja C, Pandian SK (2010) Bacillus pumilus of Palk Bay origin inhibits quorum-sensing-mediated virulence factors in Gram-negative bacteria. Res Microbiol 161:293–304
Rice SA, Koh KS, Queck SY, Labbate M, Lam KW, Kjelleberg S (2005) Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J Bacteriol 187:3477–3485
Sarah JC, Neil RW, Abigail KPH, David RS, George PCS (2006) Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorum-sensing capacities. Microbiology 152:1899–1911
Scheffer J, Konig W, Braun V, Goebel W (1998) Comparison of four hemolysin-producing organisms (Escherichia coli, Serratia marcescens, Aeromonas hydrophila and Listeria monocytogenes) for release of inflammatory mediators from various cells. J Clin Microbiol 26:544–551
Skindersoe M, Epstein EP, Rasmussen TB, Bjarnsholt T, de Rocky Nys, Givskov M (2008) Quorum sensing antagonism from marine organisms. Mar Biotechnol 10:56–63
Slater H, Crow M, Everson L, Salmond GP (2003) Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and-independent pathways. Mol Microbiol 47:303–320
Stock I, Burak S, Sherwood KJ, Gruger T, Wiedemann B (2003) Natural antimicrobial susceptibilities of strains of ‘unusual’ Serratia species: S. ficaria, S. fonticola, S. odorifera, S. plymuthica and S. rubidaea. J Antimicrob Chemother 51:865–885
Tait K, Joint I, Daykin M, Milton DL, Williams P, Camara M (2005) Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ Microbiol 7:229–240
Thenmozhi R, Nithyanand P, Rathna J, Pandian SK (2009) Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57:284–294
Traub WH (2000) Antibiotic susceptibility of Serratia marcescens and Serratia liquefaciens. Chemotherapy 46:315–321
Acknowledgments
We gratefully acknowledge the computational and bioinformatics facility provided by the Alagappa University Bioinformatics Infrastructure Facility (funded by the Department of Biotechnology, Government of India; Grant No. BT/BI/25/001/2006). A. Annapoorani gratefully acknowledges the Council of Scientific and Industrial Research (CSIR), New Delhi for the financial assistance rendered [CSIR SRF No. 9/688 (0014)/2011]. We also extend our thanks to Dr. C. Ragunathan, Zoological Survey of India, Port Blair, Andaman, India for the identification of sponges.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Annapoorani, A., Jabbar, A.K.K.A., Musthafa, S.K.S. et al. Inhibition of Quorum Sensing Mediated Virulence Factors Production in Urinary Pathogen Serratia marcescens PS1 by Marine Sponges. Indian J Microbiol 52, 160–166 (2012). https://doi.org/10.1007/s12088-012-0272-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12088-012-0272-0