Original Article

Antagonistic activities of some probiotic lactobacilli culture supernatant on Serratia marcescens swarming motility and antibiotic resistance

Abstract

Background and Objectives: Serratia marcescens, a potentially pathogenic bacterium, benefits from its swarming motility and resistance to antibiotic as two important virulence factors. Inappropriate use of antibiotics often results in drug resistance phenomenon in bacterial population. Use of probiotic bacteria has been recommended as partial replacement. In this study, we investigated the effects of some lactobacilli culture supernatant on swarming, motility and antibiotic resistance of S. marcescens.
Materials and Methods: Antimicrobial activity of lactobacilli supernatant and susceptibility testing carried out on S. marcescens isolates. Pretreatment effect of lactobacilli culture supernatant on antibiotic - resistance pattern in S. marcescens was determined by comparison of the MIC of bacteria before and after the treatment.
Results: Our results showed that pretreatment with L. acidophilus ATCC 4356 supernatant can affect the resistance of Serratia strains against ceftriaxone, but it had no effect on the resistance to other antibiotics. Furthermore, culture supernatant of lactobacilli with concentrations greater than 2%, had an effect on the swarming ability of S. marcescens ATCC 13880 and inhibited it.
Conclusion: Probiotic bacteria and their metabolites have the ability to inhibit virulence factors such as antibiotic resistance and swarming motility and can be used as alternatives to antibiotics.

Mahlen SD. Serratia infections: from military experiments to current practice. Clin Microbiol Rev 2011;24:755-791.

Jones RN. Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis 2010; 51 Suppl 1:S81-87.

Richards MJ, EdwardsJR, Culver DH, Gaynes RP. Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 2000;21:510-515.

Diekema D, Pfaller M, Jones R, Doern G, Winokur P,Gales A, et al. Survey of bloodstream infections due to Gram-negative bacilli: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, and Latin America for the SENTRY Antimicrobial Surveillance Program, 1997. Clin Infect Dis 1999;29:595-607.

Butler MT, Wang Q, Harshey RM. Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci U S A 2010;107:3776-3781.

Kearns DB. A field guide to bacterial swarming motility. Nat Rev Microbiol 2010; 8:634-644.

Overhage J, BainsM, Brazas MD, Hancock RE. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 2008;190:2671-2679.

Matsuyama T, Sogawa M, Nakagawa Y. Fractal spreading growth of Serratia marcescens which produces surface active exolipids. FEMS Microbiol Lett 1989;52:243-246.

O'Rear J, Alberti L, Harshey R. Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar function. J Bacteriol 1992;174:6125-6137.

Matsuyama T, Bhasin A, Harshey RM. Mutational analysis of flagellum-independent surface spreading of Serratia marcescens 274 on a low-agar medium. J Bacteriol 1995;177:987-991.

Lai HC, SooPC, Wei JR, Yi WC, Liaw SJ, Horng YT, et al. The RssAB two-component signal transduction system in Serratia marcescens regulates swarming motility and cell envelope architecture in response to exogenous saturated fatty acids. J Bacteriol 2005;187:3407-3414.

Wilson G, Easow JM, Mukhopadhyay C, Shivananda P. Isolation & antimicrobial susceptibility of Shigella from patients with acute gastroenteritis in western Nepal. Indian J Med Res 2006;123:145-150.

Slater H, Crow M, Everson L, Salmond GP. Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and-independent pathways. Mol Microbiol 2003;47:303-320.

Mirnejad R, Jafari H, Ardebilli A, Babavalian H. Reduction of enterotoxigenic Escherichia coli colonization by the oral administration of Lactobacillus casei as a probiotic in a murine model. Afr J Microbiol Res 2010;4:2283-2287.

Jamalifar H, Rahimi H, Samadi N, Shahverdi A, Sharifian Z, Hosseini F, et al. Reduction of enterotoxigenic Escherichia coli colonization by the oral administration of lactobacillus casei as a probiotic in a murine model. Iran J Microbiol 2011; 3:21-25.

Makras L, Triantafyllou V, Fayol-MessaoudiD, Adriany T, Zoumpopoulou G, Tsakalidou E, et al. Kinetic analysis of the antibacterial activity of probiotic lactobacilli towards Salmonella enterica serovar Typhimurium reveals a role for lactic acid and other inhibitory compounds. Res Microbiol 2006;157:241-247.

Opintan J, Newman MJ. Distribution of serogroups and serotypes of multiple drug resistant Shigella isolates. Ghana Med J 2007;41:8-29.

Lash BW, Gourama H. Microscale assay for screening of inhibitory activity of Lactobacillus. Biotechniques 2002; 33:1224-6, 1228.

Wikler M A. (2006). Clinical, Institute LS. Performance standards for antimicrobial disk susceptibility tests: approved standard.

Larson T, Peterson L, Gerding D. Microdilution aminoglycoside susceptibility testing of Pseudomonas aeruginosa and Escherichia coli: correlation between MICs of clinical isolates and quality control organisms. J Clin Microbiol 1985;22:819-821.

Ghaffari S, Varshosaz J, Saadat A, Atyabi F. Stability and antimicrobial effect of amikacin-loaded solid lipid nanoparticles. Int J Nanomedicine 2010;6:35-43.

Naderi A, Kasra-KermanshahiR, Gharavi S, Fooladi AAI, Alitappeh MA, Saffarian P. Study of antagonistic effects of Lactobacillus strains as probiotics on multi drug resistant (MDR) bacteria isolated from urinary tract infections (UTIs). Iran J Basic Med Sci 2014;17:201-208.

Shahriar M, Mawla S, Bhuiyan MA, Hossain M. Study of the effect of sodium dodecyl sulfate (SDS) and acridine orange on the isolation of plasmid and antimicrobial resistance pattern of clinical isolates of Klebsiella sp. Daffodil Int University J Sci Tech 2012;7:38-43.

Forbes BA, Daniel SF, Weissfelld AS (1998). Bailly and Scott’s Diagnostic Microbiology. 10th ed. New York.

Alberti L, Harshey RM. Differentiation of Serratia marcescens 274 into swimmer and swarmer cells. J Bacteriol 1990;172:4322-4328.

Mansouri S, Amari A, Asad AG. Inhibitory effect of some medicinal plants from Iran on swarming motility of Proteus rods. J Med Sci 2005;5:216-221.

Rodrigues AP, Holanda AR, Lustosa GP, Nobrega SM, Santana WJ, Souza LB, et al. Virulence factors and resistance mechanisms of Serratia marcescens. A short review. Acta Microbiol Immunol Hung 2006;53:89-93.

Takata N, SuginakaH, KotaniS, Ogawa M, Kosaki G. β-lactam resistance in Serratia marcescens: comparison of action of benzylpenicillin, apalcillin, cefazolin, and ceftizoxime. Antimicrob Agents Chemother 1981;19:397-401.

Alakomi HL, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander I. Lactic acid permeabilizes Gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 2000;66:2001-2005.

Taylor PW, Stapleton PD, Luzio JP. New ways to treat bacterial infections. Drug Discov Today 2002;7:1086-1091.

Roshid M, Chouduri AU. Antibacterial, anti-swarming potential of ethanol extracts of physalis minimal. Whole plant and urena lobata l. Root on cephalosporin resistant proteus species. Glob J Res Med Plants Indig Med 2014 ;3:184-195.

Ghaidaa M, Yanchang W, Abdallah H. The effect of p-nitrophenylglycerol on swarming and the production of some virulence factors in Proteus vulgaris. New York Sci J 2013;6: 8-14.

Inoue T, Shingaki R, Fukui K. Inhibition of swarming motility of Pseudomonas aeruginosa by branched-chain fatty acids. FEMS Microbiol Lett 2008;281:81-86.

Fuqua C, Greenberg EP. Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 2002;3:685-695.

Krishnan, Yin WF, Chan KG. Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa PAO1 by Ayurveda spice clove (Syzygium aromaticum) bud extract. Sensors (Basel) 2012;12:4016-4030.

Vattem DA, Mihalik K, Crixell SH, McLean RJ. Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 2007;78:302-310.

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.

Lyon GJ, Muir TW. Chemical signaling among bacteria and its inhibition. Chem Biol 2003;10:1007-1021.

Mihalik K, ChungD, CrixellS, McLean R, Vattem D. Quorum sensing modulators of Pseudomonas aeruginosa characterized in Camellia sinensis. Asian J Trad Med 2008;3:e23.

Schauder S, Bassler BL. The languages of bacteria. Genes Dev 2001;15:1468-1480.

Amrutha B, Sundar K, Shetty PH. Effect of organic acids on biofilm formation and quorum signaling of pathogens from fresh fruits and vegetables. Microb Pathog 2017;111:156-162.

Files
IssueVol 9 No 6 (2017) QRcode
SectionOriginal Article(s)
Keywords
Antibiotic resistance Probiotics Swarming Serratia marcescens

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Vahedi-Shahandashti R, Kasra-Kermanshahi R, Shokouhfard M, Ghadam P, Feizabadi MM, Teimourian S. Antagonistic activities of some probiotic lactobacilli culture supernatant on Serratia marcescens swarming motility and antibiotic resistance. Iran J Microbiol. 2018;9(6):348-355.