Staphylococcus aureus but not Listeria monocytogenes adapt to triclosan and adaptation correlates with increased fabI expression and agr deficiency

BMC Microbiology

Volumn 13, Issue 1, 2013, Pages

  Nielsen, Lene Nørby ^a   Larsen, Marianne Halberg ^a   Skovgaard, Sissel ^a,b   Kastbjerg, Vicky ^c   Westh, Henrik ^a,b   Gram, Lone ^c   Ingmer, Hanne ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b HVIDOVRE HOSPITAL   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Adaptation; Listeria monocytogenes; Staphylocooccus aureus; Triclosan

Indexed keywords

AGAR; BACTERIAL ENZYME; TRICLOSAN;

ADAPTATION; ARTICLE; BACTERIAL STRAIN; BACTERIUM COLONY; BACTERIUM ISOLATION; FATTY ACID SYNTHESIS; GRAM POSITIVE BACTERIUM; LISTERIA; LISTERIA MONOCYTOGENES; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROTEIN EXPRESSION; QUORUM SENSING; STAPHYLOCOCCUS AUREUS; VIRULENCE;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ADAPTATION, PHYSIOLOGICAL; ANTI-INFECTIVE AGENTS, LOCAL; BACTERIAL PROTEINS; FATTY ACID SYNTHASE, TYPE II; GENE EXPRESSION REGULATION, BACTERIAL; LISTERIA MONOCYTOGENES; MICROBIAL SENSITIVITY TESTS; MUTATION; STAPHYLOCOCCUS AUREUS; TRANS-ACTIVATORS; TRICLOSAN;

EID: 84880865848     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-13-177     Document Type: Article

References (50)

1. Triclosan, a commonly used bactericide found in human milk and in the aquatic environment in Sweden. Adolfsson-Erici M, Pettersson M, Parkkonen J, Sturve J, Chemosphere 2002 46 1485 1489 10.1016/S0045-6535(01)00255-7 12002480 (Pubitemid 34224476)
2. Antibacterial household products: cause for concern. Levy SB, Emerg Infect Dis 2001 7 512 515 10.3201/eid0707.017705 11485643 (Pubitemid 32726819)
3. Triclosan and antimicrobial resistance in bacteria: an overview. Yazdankhah SP, Scheie AA, Høiby EA, Lunestad B-T, Heir E, Fotland TØ Naterstad K, Kruse H, Microbial drug resistance Larchmont NY 2006 12 83 90 10.1089/mdr.2006.12.83 (Pubitemid 44162797)
4. The effectiveness of triclosan-incorporated plastic against bacteria on beef surfaces. Cutter CN, J Food Prot 1999 62 474 479 10340667 (Pubitemid 29223432)
5. Guideline for Hand Hygiene in Health-Care Settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Boyce JM, Pittet D, Infection control and hospital epidemiology the official journal of the Society of Hospital Epidemiologists of America 2002 23 3 S40 10.1086/503164 12515399
6. Impact of using triclosan-antibacterial sutures on incidence of surgical site infection. Galal I, El-Hindawy K, Am J Surg 2011 202 133 138 10.1016/j.amjsurg.2010.06.011 21600552
7. Use of perioperative mupirocin to prevent methicillin-resistant Staphylococcus aureus (MRSA) orthopaedic surgical site infections. Wilcox MH, Hall J, Pike H, Templeton PA, Fawley WN, Parnell P, Verity P, J Hosp Infect 2003 54 196 201 10.1016/S0195-6701(03)00147-6 12855234 (Pubitemid 38001992)
8. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT, Environ Sci Technol 2002 36 1202 1211 10.1021/es011055j 11944670 (Pubitemid 34228893)
9. Partitioning, persistence, and accumulation in digested sludge of the topical antiseptic triclocarban during wastewater treatment. Heidler J, Sapkota A, Halden RU, Environ Sci Technol 2006 40 3634 3639 10.1021/es052245n 16786704 (Pubitemid 43830972)
10. Detection of the antimicrobials triclocarban and triclosan in agricultural soils following land application of municipal biosolids. Cha J, Cupples AM, Water Res 2009 43 2522 2530 10.1016/j.watres.2009.03.004 19327812
11. Snail bioaccumulation of triclocarban, triclosan, and methyltriclosan in a North Texas, USA, stream affected by wastewater treatment plant runoff. Coogan MA, La Point TW, Environ Toxicol Chem 2008 27 1788 1793 10.1897/07-374.1 18380516
12. Environmental Exposure of Aquatic and Terrestrial Biota to Triclosan and Triclocarban. Chalew TE, Halden RU, J Am Water Works Assoc 2009 45 4 13 10.1111/j.1752-1688.2008.00284.x 20046971
13. Reduced Susceptibility of Proteus mirabilis to triclosan. Stickler DJ, Jones GL, Antimicrob Agents Chemother 2008 52 991 994 10.1128/AAC.01094-07 18180352 (Pubitemid 351358378)
14. Microarray analysis of toxicogenomic effects of triclosan on Staphylococcus aureus. Jang H-J, Chang MW, Toghrol F, Bentley WE, Appl Microbiol Biotechnol 2008 78 695 707 10.1007/s00253-008-1349-x 18210102
15. Triclosan targets lipid synthesis. McMurry LM, Oethinger M, Levy SB, Nature 1998 394 531 532 10.1038/28970 9707111 (Pubitemid 28366816)
16. Inhibition of the Staphylococcus aureus NADPH-dependent enoyl-acyl carrier protein reductase by triclosan and hexachlorophene. Heath RJ, Li J, Roland GE, Rock CO, J Biol Chem 2000 275 4654 4659 10.1074/jbc.275.7.4654 10671494 (Pubitemid 30108851)
17. Triclosan-bacteria interactions: single or multiple target sites? Escalada MG, Russell AD, Maillard J-Y, Ochs D, Lett Appl Microbiol 2005 41 476 481 10.1111/j.1472-765X.2005.01790.x 16305673 (Pubitemid 41735618)
18. Membranotropic effects of the antibacterial agent Triclosan. Villalaín J, Mateo CR, Aranda FJ, Shapiro S, Micol V, Arch Biochem Biophys 2001 390 128 136 10.1006/abbi.2001.2356 11368524 (Pubitemid 32493578)
19. Triclosan-resistant Staphylococcus aureus. Sasatsu M, Shimizu K, Noguchi N, Kono M, Lance 1993 341 756
20. Transferable resistance to triclosan in MRSA. Cookson BD, Farrelly H, Stapleton P, Garvey RP, Price MR, Lance 1991 337 1548 1549
21. An assessment of triclosan susceptibility in methicillin-resistant and methicillin-sensitive Staphylococcus aureus. Bamber AI, Neal TJ, J Hosp Infect 1999 41 107 109 10.1016/S0195-6701(99)90047-6 10063472 (Pubitemid 29084004)
22. Triclosan and antibiotic resistance in Staphylococcus aureus. Suller MT, Russell AD, J Antimicrob Chemother 2000 46 11 18 10997594 (Pubitemid 30466190)
23. Antibiotic and biocide resistance in methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococcus. Suller MT, Russell AD, J Hosp Infect 1999 43 281 291 10.1016/S0195-6701(99)90424-3 10658804 (Pubitemid 30045827)
24. Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis. Heath RJ, Yu YT, Shapiro MA, Olson E, Rock CO, J Biol Chem 1998 273 30316 30320 10.1074/jbc.273.46.30316 9804793 (Pubitemid 28545500)
25. Defining and Combating the Mechanisms of Triclosan Resistance in Clinical Isolates of Staphylococcus aureus. Fan F, Yan K, Wallis NG, Reed S, Moore TD, Rittenhouse SF, Dewolf WE, Huang J, Mcdevitt D, Miller WH, Seefeld MA, Newlander KA, Jakas DR, Head MS, Payne DJ, Al FANET, Society 2002 46 3343 3347 (Pubitemid 35192895)
26. Triclosan resistance in Salmonella enterica serovar Typhimurium. Webber MA, Randall LP, Cooles S, Woodward MJ, Piddock LJV, J Antimicrob Chemother 2005 56 83 91
27. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. McMurry LM, Oethinger M, Levy SB, FEMS Microbiol Lett 1998 166 305 309 10.1111/j.1574-6968.1998.tb13905. x 9770288 (Pubitemid 128384175)
28. Differential network expression during drug and stress response. Cabusora L, Sutton E, Fulmer A, Forst CV, Bioinformatics 2005 21 2898 2905 10.1093/bioinformatics/bti440 15840709 (Pubitemid 40862290)
29. A triclosan-ciprofloxacin cross-resistant mutant strain of Staphylococcus aureus displays an alteration in the expression of several cell membrane structural and functional genes. Tkachenko O, Shepard J, Aris VM, Joy A, Bello A, Londono I, Marku J, Soteropoulos P, Peteroy-Kelly MA, Res Microbiol 2007 158 651 658 10.1016/j.resmic.2007.09.003 17997080 (Pubitemid 350213379)
30. High-Level Fluoroquinolone-Resistant Clinical Isolates of Escherichia coli Overproduce Multidrug Efflux Protein AcrA. Mazzariol A, Tokue Y, Kanegawa TM, Cornaglia G, Nikaido H, Antimicrob Agents Chemother 2000 44 3441 3443 10.1128/AAC.44.12.3441-3443.2000 11083655 (Pubitemid 33009509)
31. Small-colony variants: a novel mechanism for triclosan resistance in methicillin-resistant Staphylococcus aureus. Seaman PF, Ochs D, Day MJ, J Antimicrob Chemother 2007 59 43 50 17079243 (Pubitemid 46017899)
32. Sublethal Triclosan Exposure Decreases Susceptibility to Gentamicin and Other Aminoglycosides in Listeria monocytogenes. Christensen EG, Gram L, Kastbjerg VG, Antimicrob Agents Chemother 2011 55 4064 4071 10.1128/AAC.00460-11 21746948
33. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Novick R, Virology 1967 33 155 66 10.1016/0042-6822(67) 90105-5 4227577
34. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-remington F, Online 2006 367 731 739 (Pubitemid 43326291)
35. Epidemic listeriosis associated with Mexican-style cheese. Linnan MJ, Mascola L, Lou XD, Goulet V, May S, Salminen C, Hird DW, Yonekura ML, Hayes P, Weaver R, N Engl J Med 1988 319 823 8 10.1056/NEJM198809293191303 3137471
36. One group of genetically similar Listeria monocytogenes strains frequently dominates and persists in several fish slaughter- and smokehouses. Wulff G, Gram L, Ahrens P, Vogel BF, Appl Environ Microbiol 2006 72 4313 22 10.1128/AEM.02288-05 16751546 (Pubitemid 43898662)
37. Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. Kastbjerg VG, Gram L, Int J Food Microbiol 2012 160 11 15 10.1016/j.ijfoodmicro.2012.09.009 23141640
38. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG, J Clin Microbiol 2000 38 1008 1015 10698988 (Pubitemid 30140551)
39. Biochemical and genetic characterization of the action of triclosan on Staphylococcus aureus. Slater-radosti C, Van AG, Greenwood R, Nicholas R, Keller PM, Dewolf WE, Fan F, Payne DJ, Jaworski DD, J Antimicrob Chemother 2001 48 1 6 11566971 (Pubitemid 32684718)
40. Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Frees D, Chastanet A, Qazi S, Sørensen K, Hill P, Msadek T, Ingmer H, Mol Microbiol 2004 54 1445 1462 10.1111/j.1365-2958.2004.04368.x 15554981 (Pubitemid 39578284)
41. A Nonsense Mutation in agrA Accounts for the Defect in agr Expression and the Avirulence of Staphylococcus aureus 8325-4 traP::kan. Adhikari RP, Arvidson S, Novick RP, Infect Immun 2007 75 4534 4540 10.1128/IAI.00679-07 17606604 (Pubitemid 47378114)
42. Widespread Distribution of Disinfectant Resistance Genes among Staphylococci of Bovine and Caprine Origin in Norway. Bjorland J, Steinum T, Kvitle B, Waage S, Sunde M, Heir E, J Clin Microbiol 2005 43 4363 4368 10.1128/JCM.43.9.4363-4368.2005 16145078 (Pubitemid 41298214)
43. Community-associated MRSA-resistance and virulence converge. Chambers HF, N Engl J Med 2005 352 1485 7 10.1056/NEJMe058023 15814886 (Pubitemid 40471458)
44. Efflux-mediated response of Staphylococcus aureus exposed to ethidium bromide. Couto I, Costa SS, Viveiros M, Martins M, Amaral L, J Antimicrob Chemother 2008 62 504 513 10.1093/jac/dkn217 18511413
45. A novel resistance mechanism to triclosan that suggests horizontal gene transfer and demonstrates a potential selective pressure for reduced biocide susceptibility in clinical strains of Staphylococcus aureus. Ciusa ML, Furi L, Knight D, Decorosi F, Fondi M, Raggi C, Coelho JR, Aragones L, Moce L, Visa P, Freitas AT, Baldassarri L, Fani R, Viti C, Orefici G, Martinez JL, Morrissey I, Oggioni MR, Int J Antimicrob Agents 2012 40 210 220 10.1016/j.ijantimicag.2012. 04.021 22789727
46. Staphylococcus aureus FabI: inhibition, substrate recognition, and potential implications for in vivo essentiality. Schiebel J, Chang A, Lu H, Baxter MV, Tonge PJ, Kisker C, Structure (London, England: 1993) 2012 20 802 13 10.1016/j.str.2012.03.013
47. Triclosan resistance in methicillin-resistant Staphylococcus aureus expressed as small colony variants: a novel mode of evasion of susceptibility to antiseptics. Bayston R, Ashraf W, Smith T, J Antimicrob Chemother 2007 59 43 50 17079243
48. Virulence of Staphylococcus aureus Small Colony Variants in the Caenorhabditis elegans Infection Model. Sifri CD, Baresch-Bernal A, Calderwood SB, Von Eiff C, Infect Immun 2006 74 1091 1096 10.1128/IAI.74.2.1091-1096.2006 16428756 (Pubitemid 43185546)
49. Attenuated virulence and biofilm formation in Staphylococcus aureus following sublethal exposure to triclosan. Latimer J, Forbes S, McBain AJ, Antimicrob Agents Chemother 2012 56 3092 100 10.1128/AAC.05904-11 22430975
50. Triclosan-tolerant bacteria: changes in susceptibility to antibiotics. Cottell A, Denyer S, Hanlon GW, Ochs D, Maillard JY, J Hosp Infect 2009 72 71 76 10.1016/j.jhin.2009.01.014 19246121