Altered competitive fitness, antimicrobial susceptibility, and cellular morphology in a triclosan-induced small-colony variant of Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 8, 2015, Pages 4809-4816

  Forbes, Sarah ^a   Latimer, Joe ^a   Bazaid, Abdulrahman ^a   McBain, Andrew J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACTERIAL PROTEIN; BENZALKONIUM CHLORIDE; CEFALOTIN; CHLORHEXIDINE; CIPROFLOXACIN; COTRIMOXAZOLE; FABI PROTEIN; GENTAMICIN; GLYCOSYLTRANSFERASE; ISAA PROTEIN; KANAMYCIN; MICROBICIDE; POLY(HEXAMETHYLENEBIGUANIDE); TETRACYCLINE; TRICLOSAN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL SURVIVAL; BACTERIUM COLONY; CELL DIVISION; CELL STRUCTURE; CONTROLLED STUDY; DISK DIFFUSION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTIVE FITNESS; STAPHYLOCOCCUS AUREUS; DRUG EFFECTS; GENETICS; MICROBIAL SENSITIVITY TEST; PHENOTYPE; PROCEDURES; PROTEOMICS; STAPHYLOCOCCAL INFECTIONS; UPREGULATION;

ANTI-INFECTIVE AGENTS; BACTERIAL PROTEINS; CELL DIVISION; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; PHENOTYPE; PROTEOMICS; STAPHYLOCOCCAL INFECTIONS; TRICLOSAN; UP-REGULATION;

EID: 84939832782     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00352-15     Document Type: Article

References (45)

1. von Eiff C, Heilmann C, Proctor RA, Woltz C, Peters G, Götz F. 1997. A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 179:4706-4712.
2. Proctor RA, van Langevelde P, Kristjansson M, Maslow JN, Arbeit RD. 1995. Persistent and relapsing infections associated with small-colony variants of Staphylococcus aureus. Clin Infect Dis 20:95-102. http://dx.doi.org/10.1093/clinids/20.1.95.
3. Schaaff F, Bierbaum G, Baumert N, Bartmann P, Sahl HG. 2003. Mutations are involved in emergence of aminoglycoside-induced small colony variants of Staphylococcus aureus. Int J Med Microbiol 293:427-435. http://dx.doi.org/10.1078/1438-4221-00282.
4. Abu-Qatouseh LF, Chinni SV, Seggewiß J, Proctor RA, Brosius J, Rozhdestvensky TS, Peters G, von Eiff C, Becker K. 2010. Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype. J Mol Med 88:565-575. http://dx.doi.org/10.1007/s00109-010-0597-2.
5. Tuchscherr L, Heitmann V, Hussain M, Viemann D, Roth J, von Eiff C, Peters G, Becker K, Löffler B. 2010. Staphylococcus aureus small-colony variants are adapted phenotypes for intracellular persistence. J Infect Dis 202:1031-1040. http://dx.doi.org/10.1086/656047.
6. Latimer J, Forbes S, McBain AJ. 2012. Attenuated virulence and biofilm formation in Staphylococcus aureus following sublethal exposure to triclosan. Antimicrob Agents Chemother 56:3092-3100. http://dx.doi.org/10.1128/AAC.05904-11.
7. Brouillette E, Martinez A, Boyll BJ, Allen NE, Malouin F. 2004. Persistence of a Staphylococcus aureus small-colony variant under antibiotic pressure in vivo. FEMS Immunol Med Microbiol 41:35-41. http://dx.doi.org/10.1016/j.femsim.2003.12.007.
8. Gläser R, Becker K, von Eiff C, Meyer-Hoffert U, Harder J. 2014. Decreased susceptibility of Staphylococcus aureus small colony variants (SCVs) towards human antimicrobial peptides. J Investig Dermatol 134:2347-2350. http://dx.doi.org/10.1038/jid.2014.176.
9. Kahl B, Herrmann M, Everding AS, Koch HG, Becker K, Harms E, Proctor RA, Peters G. 1998. Persistent infection with small colony variant strains of Staphylococcus aureus in patients with cystic fibrosis. J Infect Dis 177:1023-1029. http://dx.doi.org/10.1086/515238.
10. Sendi P, Rohrbach M, Graber P, Frei R, Ochsner PE, Zimmerli W. 2006. Staphylococcus aureus small colony variants in prosthetic joint infection. Clin Infect Dis 43:961-967. http://dx.doi.org/10.1086/507633.
11. Lannergård J, von Eiff C, Sander G, Cordes T, Seggewiß J, Peters G, Proctor RA, Becker K, Hughes D. 2008. Identification of the genetic basis for clinical menadione-auxotrophic small-colony variant isolates of Staphylococcus aureus. Antimicrob Agents Chemother 52:4017-4022. http://dx.doi.org/10.1128/AAC.00668-08.
12. von Eiff C, McNamara P, Becker K, Bates D, Lei X-H, Ziman M, Bochner BR, Peters G, Proctor RA. 2006. Phenotype microarray profiling of Staphylococcus aureus menD and hemB mutants with the small-colony-variant phenotype. J Bacteriol 188:687-693. http://dx.doi.org/10.1128/JB.188.2.687-693.2006.
13. Kahl BC, Belling G, Reichelt R, Herrmann M, Proctor RA, Peters G. 2003. Thymidine-dependent small-colony variants of Staphylococcus aureus exhibit gross morphological and ultrastructural changes consistent with impaired cell separation. J Clin Microbiol 41:410-413. http://dx.doi.org/10.1128/JCM.41.1.410-413.2003.
14. von Eiff C, Proctor RA, Peters G. 2000. Small colony variants of staphylococci: a link to persistent infections. Berl Munch Tierarztl Wochenschr 113:321-325.
15. Besier S, Ludwig A, Ohlsen K, Brade V, Wichelhaus TA. 2007. Molecular analysis of the thymidine-auxotrophic small colony variant phenotype of Staphylococcus aureus. Int J Med Microbiol 297:217-225. http://dx.doi.org/10.1016/j.ijmm.2007.02.003.
16. Schnitzer RJ, Camagni LJ, Buck M. 1943. Resistance of small colony variants (G-forms) of a staphylococcus towards the bacteriostatic activity of penicillin. Exp Biol Med 53:75-78. http://dx.doi.org/10.3181/00379727-53-14192.
17. Gilman S, Saunders VA. 1986. Accumulation of gentamicin by Staphylococcus aureus: the role of the transmembrane electrical potential. J Antimicrob Chemother 17:37-44. http://dx.doi.org/10.1093/jac/17.1.37.
18. Besier S, Zander J, Kahl BC, Kraiczy P, Brade V, Wichelhaus TA. 2008. The thymidine-dependent small-colony-variant phenotype is associated with hypermutability and antibiotic resistance in clinical Staphylococcus aureus isolates. Antimicrob Agents Chemother 52:2183-2189. http://dx.doi.org/10.1128/AAC.01395-07.
19. Balwit JM, Van Langevelde P, Vann JM, Proctor RA. 1994. Gentamicin-resistant menadione and hemin auxotrophic Staphylococcus aureus persist within cultured endothelial cells. J Infect Dis 170:1033-1037. http://dx.doi.org/10.1093/infdis/170.4.1033.
20. Nguyen HA, Denis O, Vergison A, Theunis A, Tulkens PM, Struelens MJ, Van Bambeke F. 2009. Intracellular activity of antibiotics in a model of human THP-1 macrophages infected by a Staphylococcus aureus small-colony variant strain isolated from a cystic fibrosis patient: pharmacodynamic evaluation and comparison with isogenic normal-phenotype and revertant strains. Antimicrob Agents Chemother 53:1434-1442. http://dx.doi.org/10.1128/AAC.01145-08.
21. Kohler C, von Eiff C, Peters G, Proctor RA, Hecker M, Engelmann S. 2003. Physiological characterization of a heme-deficient mutant of Staphylococcus aureus by a proteomic approach. J Bacteriol 185:6928-6937. http://dx.doi.org/10.1128/JB.185.23.6928-6937.2003.
22. Rozen DE, McGee L, Levin BR, Klugman KP. 2007. Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 51:412-416. http://dx.doi.org/10.1128/AAC.01161-06.
23. Levin BR, Perrot V, Walker N. 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154:985-997.
24. Bayston R, Ashraf W, Smith T. 2007. Triclosan resistance in methicillin-resistant Staphylococcus aureus expressed as small colony variants: a novel mode of evasion of susceptibility to antiseptics. J Antimicrob Chemother 59:848-853. http://dx.doi.org/10.1093/jac/dkm031.
25. Seaman PF, Ochs D, Day MJ. 2007. Small-colony variants: a novel mechanism for triclosan resistance in methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 59:43-50.
26. Barbolt TA. 2002. Chemistry and safety of triclosan, and its use as an antimicrobial coating on coated VICRYL Plus antibacterial suture (coated polyglactin 910 suture with triclosan). Surg Infect 3:s45-s53. http://dx.doi.org/10.1089/sur.2002.3.s1-45.
27. Moran J, Addy M, Newcombe R, Marlow I. 2001. A study to assess the plaque inhibitory action of a newly formulated triclosan toothpaste. J Clin Periodontol 28:86-89. http://dx.doi.org/10.1034/j.1600-051x.2001.280113.x.
28. Faoagali J, Fong J, George N, Mahoney P, O'Rourke V. 1995. Comparison of the immediate, residual, and cumulative antibacterial effects of Novaderm R, Novascrub R, Betadine Surgical Scrub, Hibiclens, and liquid soap. Am J Infect Control 23:337-343. http://dx.doi.org/10.1016/0196-6553(95)90263-5.
29. Levy CW, Roujeinikova A, Sedelnikova S, Baker PJ, Stuitje AR, Slabas AR, Rice DW, Rafferty JB. 1999. Molecular basis of triclosan activity. Nature 398:383-384. http://dx.doi.org/10.1038/18803.
30. McMurry LM, Oethinger M, Levy SB. 1998. Triclosan targets lipid synthesis. Nature 394:531-532. http://dx.doi.org/10.1038/28970.
31. Heath RJ, Rock CO. 2000. Microbiology: a triclosan-resistant bacterial enzyme. Nature 406:145-146. http://dx.doi.org/10.1038/35018162.
32. Villalain J, Mateo CR, Aranda FJ, Shapiro S, Micol V. 2001. Membranotropic effects of the antibacterial agent triclosan. Arch Biochem Biophys 390:128-136. http://dx.doi.org/10.1006/abbi.2001.2356.
33. Ledder RG, Gilbert P, Willis C, McBain AJ. 2006. Effects of chronic triclosan exposure upon the antimicrobial susceptibility of 40 ex-situ environmental and human isolates. J Appl Microbiol 100:1132-1140. http://dx.doi.org/10.1111/j.1365-2672.2006.02811.x.
34. McMurry LM. 1998. Triclosan targets lipid synthesis. Nature 394:531. http://dx.doi.org/10.1038/28970.
35. McMurry LM. 1998. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol Lett 166:305. http://dx.doi.org/10.1111/j.1574-6968.1998.tb13905.x.
36. Sanchez P. 2005. The biocide triclosan selects Stenotrophomonas maltophilia mutants that overproduce the SmeDEF multidrug efflux pump. Antimicrob Agents Chemother 49:781. http://dx.doi.org/10.1128/AAC.49.2.781-782.2005.
37. Moore LE, Ledder RG, Gilbert P, McBain AJ. 2008. In vitro study of the effect of cationic biocides on bacterial population dynamics and susceptibility. Appl Environ Microbiol 74:4825. http://dx.doi.org/10.1128/AEM.00573-08.
38. Andrews JM, BSAC Working Party on Susceptibility Testing. 2001. BSAC standardized disc susceptibility testing method. J Antimicrob Chemother 48:43-57. http://dx.doi.org/10.1093/jac/48.suppl-1.43.
39. Paulander W, Varming AN, Bæk KT, Haaber J, Frees D, Ingmer H. 2013. Antibiotic-mediated selection of quorum-sensing-negative Staphylococcus aureus. mBio 3(6):e00459-12. http://dx.doi.org/10.1128/mBio.00459-12.
40. Margolis PS. 2000. Peptide deformylase in Staphylococcus aureus: resistance to inhibition is mediated by mutations in the formyltransferase gene. Antimicrob Agents Chemother 44:1825. http://dx.doi.org/10.1128/AAC.44.7.1825-1831.2000.
41. Stapleton MR. 2007. Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J Bacteriol 189:7316. http://dx.doi.org/10.1128/JB.00734-07.
42. Chuard C, Vaudaux PE, Proctor RA, Lew DP. 1997. Decreased susceptibility to antibiotic killing of a stable small colony variant of Staphylococcus aureus in fluid phase and on fibronectin-coated surfaces. J Antimicrob Chemother 39:603-608. http://dx.doi.org/10.1093/jac/39.5.603.
43. Kunz AN, Begum AA, Wu H, D'Ambrozio JA, Robinson JM, Shafer WM, Bash MC, Jerse AE. 2012. Impact of fluoroquinolone resistance mutations on gonococcal fitness and in vivo selection for compensatory mutations. J Infect Dis 205:1821-1829. http://dx.doi.org/10.1093/infdis/jis277.
44. Andersson DI, Levin BR. 1999. The biological cost of antibiotic resistance. Curr Opin Microbiol 2:489-493. http://dx.doi.org/10.1016/S1369-5274(99)00005-3.
45. Guo B, Abdelraouf K, Ledesma KR, Nikolaou M, Tam VH. 2012. Predicting bacterial fitness cost associated with drug resistance. J Antimicrob Chemother 67:928-932. http://dx.doi.org/10.1093/jac/dkr560.