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Adaptation to benzalkonium chloride and ciprofloxacin affects biofilm formation potential, efflux pump and haemolysin activity of Escherichia coli of dairy origin

Published online by Cambridge University Press:  06 July 2012

Ankita Pagedar*
Affiliation:
Dairy Microbiology Division, National Dairy Research Institute (NDRI), Karnal (Haryana) 132001, India Present Address: Department of Microbiology, Ashok and Rita Patel Institute of Integrated Studies and Research in Biotechnology and Allied Sciences (ARIBAS), New Vallabh Vidya Nagar-388121, Gujarat, India
Jitender Singh
Affiliation:
Dairy Microbiology Division, National Dairy Research Institute (NDRI), Karnal (Haryana) 132001, India Present Address: Product and Process Development Group, National Dairy Development Board (NDDB), Anand-388001, Gujarat, India
Virender K. Batish
Affiliation:
Dairy Microbiology Division, National Dairy Research Institute (NDRI), Karnal (Haryana) 132001, India
*
*For correspondence; e-mail: ankitapagedar@gmail.com

Abstract

The present study investigates the effect of adaptive resistance to ciprofloxacin (Cip) and benzalkonium chloride (BC) on biofilm formation potential (BFP), efflux pump activity (EPA) and haemolysin activity of Escherichia coli isolates of dairy origin. All the isolates, irrespective of antimicrobial susceptibility, developed significant adaptive resistance (P < 0·05). All the resistant phenotypes (antibiotic resistant: AR; & biocide resistant: BR) were stronger biofilm former and post-adaptation, an insignificant change was observed in their BFP. Whereas, post-adaptation, non-resistant isolates (antibiotic non-resistant: ANR; biocide non-resistant: BNR) transformed from poor or moderate to strong biofilm formers. Post-adaptive percentage increase in EPA was highly significant in non-resistant categories (P < 0·01) and significant at P < 0·05 in BR category. Interestingly, post-adaptive increase in EPA in BR isolates was more than that in AR yet, the latter exhibited greater adaptive resistance than the former. These findings indicated prevalence of some other specific resistance mechanism/s responsible for adaptive resistance against Cip. Strain specific variations were observed for stability of adaptive resistance and haemolysin activity for all the categories. Our findings especially in reference to post-adaptation upgradation of BFP status of non-resistant isolates seems to be providing an insight into the process of conversion of non-resistant isolate into resistant ones with enhanced BFP. These observations emphasize the serious implications of sub-lethal residual levels of antimicrobials in food environments and suggest a role of food chain in emergence of antimicrobial resistances.

Type
Research Article
Copyright
Copyright © Proprietors of Journal of Dairy Research 2012

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References

Arias, A, Seral, C, Gude, MJ & Castillo, FJ 2010 Molecular mechanisms of quinolone resistance in clinical isolates of Aeromonas caviae and Aeromonas veronii bv. Sobria. International Microbiology 13 135141Google Scholar
Bohnert, JA, Schuster, S, Fahnrich, E, Trittler, R & Kern, WV 2007 Altered spectrum of multidrug resistance associated with a single point mutation in the Escherichia coli RND-type MDR efflux pump YhiV (MdtF). Journal of Antimicrobial Chemotherapy 59 12161222Google Scholar
Bore, E, Hébraud, M, Chafsey, I, Chambon, C, Skjaeret, C, Moen, B, Møretrø, T, Langsrud, Ø, Rudi, K & Langsrud, S 2007 Adapted tolerance to benzalkonium chloride in Escherichia coli K-12 studied by transcriptome and proteome analyses. Microbiology 153 935946Google Scholar
Brown, MRW & Gilbert, P 1993 Sensitivity of biofilms to antimicrobial agents. Journal of Applied Bacteriology 74 87S97SGoogle Scholar
Clinical and Lab Standards Institute (CLSI) 2011 Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard—Eighth Edition. M07-A8. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement M100-S21 31(1). Clinical and Lab Standards Institute, Wayne, Pennsylvania, USAGoogle Scholar
Drenkard, E & Ausubel, FM 2002 Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416 740743Google Scholar
Gualdi, L, Tagliabue, L & Landini, P 2007 Biofilm formation-gene expression relay system in Escherichia coli: modulation of sigmaS-dependent gene expression by the CsgD regulatory protein via sigmaS protein stabilization. Journal of Bacteriology 189 80348043Google Scholar
Hengge, R 2009 Proteolysis of σS (RpoS) and the general stress response in Escherichia coli. Research in Microbiology 160 667676CrossRefGoogle ScholarPubMed
Horcajada, JP, Soto, S, Gajewski, A, Smithson, A, Jimenez de Anta, MT, Mensa, J, Vila, J & Johnson, JR 2005 Quinolone resistant uropathogenic Escherichia coli strains from phylogenetic group B2 have fewer virulence factors than their susceptible counterparts. Journal of Clinical Microbiology 43 29622964Google Scholar
Imuta, N, Nishi, J, Tokuda, K, Fujiyama, R, Manago, K, Iwashita, M, Sarantuya, J & Kawano, Y 2008 The Escherichia coli efflux pump TolC promotes aggregation of enteroaggregative Esch. coli 042. Infection and Immunity 76 12471256Google Scholar
Johnson, JR, Kuskowski, MA, Gajewski, A, Soto, S, Horcajada, JP, Jimenez de Anta, MT & Vila, J 2005 Extended virulence genotypes and phyelonephritis or prostatitis. Journal of Infectious Disease 191 4650Google Scholar
Kendall, MM & Sperandio, V 2007 Quorum sensing by enteric pathogens. Current Opinion Gastroenterology 23 1015Google Scholar
Langsrud, S, Sundheim, G & Holck, AL 2004 Cross-resistance to antibiotics of Escherichia coli adapted to benzalkonium chloride or exposed to stress-inducers. Journal of Applied Microbiology 96 201208Google Scholar
Ma, D, Alberti, M, Lynch, C, Nikaido, H & Hearst, JE 1996 The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Molecular Microbiology 19 101112Google Scholar
Machado, I, Lopes, SP, Sousa, AM & Pereira, MO 2012 Adaptive response of single and binary Pseudomonas aeruginosa and Escherichia coli biofilms to benzalkonium chloride. Journal of Basic Microbiology 52 4352Google Scholar
Marhova, M, Kostadinova, S & Stoitsova, S 2010 Biofilm-forming capabilities of urinary Escherichia coli isolates. Biotechnology 24 589593Google Scholar
Naves, P, del Prado, G, Huelves, L, Gracia, M, Ruiz, V, Blanco, J, Dahbi, G, Blanco, M, del Carmen Ponte, M & Soriano, F 2008 Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microbial Pathogenesis 45 8691Google Scholar
Ntsama-Essomba, C, Bouttier, S, Ramaldes, M, Dubois-Brissonnet, F & Fourniat, J 1997 Resistance of Escherichia coli growing as biofilms to disinfectants. Veterinary Research 28 353363Google Scholar
Pagedar, A, Singh, J & Batish, VK 2010 Surface hydrophobicity, nutritional contents affect Staphylococcus aureus biofilms and temperature influences its survival in preformed biofilms. Journal of Basic Microbiology 50(S1) 98106CrossRefGoogle ScholarPubMed
Pagedar, A, Singh, J & Batish, VK 2011 Efflux mediated adaptive and cross resistance to ciprofloxacin and benzalkonium chloride in Pseudomonas aeruginosa of dairy origin. Journal of Basic Microbiology 51 289295Google Scholar
Piatti, G, Mannini, A, Balistreri, M & Schito, AM 2008 Virulence factors in urinary Escherichia coli strains: phylogenetic background and quinolone and fluoroquinolone resistance. Journal of Clinical Microbiology 46 480487Google Scholar
Qu, Y, Daley, AJ, Istivan, TS, Garland, SM & Deighton, MA 2010 Antibiotic susceptibility of coagulase-negative staphylococci isolated from very low birth weight babies: comprehensive comparisons of bacteria at different stages of biofilm formation. Annals of Clinical Microbiology and Antimicrobials 27 916Google Scholar
Raherison, S, Gonzalez, P, Renaudin, H, Charron, A, Bébéar, C & Bébéar, CM 2002 Evidence of active efflux in resistance to ciprofloxacin and to ethidium bromide by Mycoplasma hominis. Antimicrobial Agents and Chemotherapy 46 672679Google Scholar
Rijavec, M, Muller-Premru, M, Zakotnik, B & Zgur-Bertok, D 2008 Virulence factors and biofilm production among Escherichia coli strains causing bacteraemia of urinary tract origin. Journal of Medical Microbiology 57 13291334Google Scholar
Romanova, NA, Gawande, PV, Brovko, LY & Griffiths, MW 2007 Rapid methods to assess sanitizing efficacy of benzalkonium chloride to Listeria monocytogenes biofilms. Journal of Microbiological Methods 71 231237Google Scholar
Skals, M, Jorgensen, NR, Leipziger, J & Praetorius, HA 2009 α-Haemolysin from Escherichia coli uses endogenous amplification through P2X receptor activation to induce hemolysis. Proceedings of National Academy Science, USA 106 40304035Google Scholar
Soto, SM, Smithson, A, Martinez, JA, Horcajada, JP, Mensa, J & Vila, J 2007 Biofilm formation in uropathogenic Escherichia coli strains: Relationship with prostatitis, urovirulence factors and antimicrobial resistance. Journal of Urology 177 365368Google Scholar
Tiwari, RP, Deol, K, Rishi, P & Grewal, JS 2002 Factors affecting haemolysin production and Congo red binding in Salmonella enterica serovar Typhimurium DT 98. Journal of Medical Microbiology 51 503509Google Scholar
van der Horst, MA, Schuurmans, JM, Smid, MC, Koenders, BB & Ter Kuile, BH 2011 De novo acquisition of resistance to three antibiotics by Escherichia coli. Microbial Drug Resistance 17 141147Google Scholar
Van der Veen, S & Abee, T 2010 Importance of SigB for Listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Applied Environmental Microbiology 76 7854.Google Scholar
Velázquez, LC, Barbini, NB, Escudero, ME, Estrada, CL & de Guzmán, AMS 2009 Evaluation of chlorine, benzalkonium chloride and lactic acid as sanitizers for reducing Escherichia coli O157:H7 and Yersinia enterocolitica on fresh vegetables. Food Control 20 262268Google Scholar