Characterization of triclosan-resistant mutants reveals multiple antimicrobial resistance mechanisms in rhodospirillum rubrum S1H

Applied and Environmental Microbiology

Volumn 76, Issue 10, 2010, Pages 3116-3123

  Pycke, Benny F G ^a,b,c   Crabbé, Aurélie ^b,c   Verstraete, Willy ^a   Leys, Natalie ^b  

^a GHENT UNIVERSITY   (Belgium)

^b BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL RESISTANCES; CARBENICILLIN; CELL PERMEABILIZATION; DEFENSE MECHANISM; EFFLUX PUMPS; EXPOSURE CONCENTRATION; GENOTYPING; MEMBRANE PERMEABILITY; MICROPOLLUTANTS; PARENT STRAIN; POINT MUTATIONS; RESISTANCE PROFILES; RESISTANT MUTANTS; RHODOSPIRILLUM RUBRUM; TRANSCRIPTIONAL ANALYSIS; TRICLOSAN; UP-REGULATION;

MICROORGANISMS;

ANTIBIOTICS;

ANTIINFECTIVE AGENT; ENOYL ACYL CARRIER PROTEIN REDUCTASE (NADH); TRICLOSAN;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; BACTERIUM; GENOTYPE; MEMBRANE; MUTATION; PERMEABILITY; PESTICIDE RESISTANCE;

ANTIBIOTIC RESISTANCE; ARTICLE; BIOLOGY; DRUG EFFECT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGICAL EXAMINATION; MUTATION; RHODOSPIRILLUM RUBRUM;

ANTI-BACTERIAL AGENTS; COMPUTATIONAL BIOLOGY; DRUG RESISTANCE, BACTERIAL; ENOYL-(ACYL-CARRIER-PROTEIN) REDUCTASE (NADH); MICROBIAL SENSITIVITY TESTS; MUTATION; RHODOSPIRILLUM RUBRUM; TRICLOSAN;

RHODOSPIRILLUM RUBRUM;

EID: 77952270258     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02757-09     Document Type: Article

References (44)

1. Aiello, A. E., B. Marshall, S. B. Levy, P. Della-Latta, and E. Larson. 2004. Relationship between triclosan and susceptibilities of bacteria isolated from hands in the community. Antimicrob. Agents Chemother. 48:2973-2979.
2. Balsalobre, C., J. Calonge, E. Jiménez, R. Lafuente, M. Mouriño, M. T. Muñoz, M. Riquelme, and J. Mascastellà. 2006. Using the metabolic capacity of Rhodobacter sphaeroides to assess heavy metal toxicity. Environ. Toxicol. Water Qual. 8: 437-450.
3. Birosova, L., and M. Mikulasova. 2009. Development of triclosan and antibiotic resistance in Salmonella entérica serovar Typhimurium. J. Med. Microbiol. 58:436-441.
4. Bordello, G., E. Werner, F. Roe, A. M. Kim, G. D. Ehrlich, and P. S. Stewart. 2004. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 48:2659-2664.
5. Braoudaki, M., and A. C. Hilton. 2004. Adaptive resistance to biocides in Salmonella entérica and Escherichia coli 0157 and cross-resistance to antimicrobial agents. J. Clin. Microbiol. 42:73-78.
6. Braoudaki, M., and A. C. Hilton. 2004. Low level of cross-resistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli 055 compared to E. coli 0157. FEMS Microbiol. Lett. 235:305-309. (Pubitemid 38746776)
7. Bron, S., and G. Venema. 1972. Ultraviolet inactivation and excision-repair in Bacillus subtillis. Construction of a transformable 8-fold auxotrophic strain and to ultra-violet sensitive derivatives. Mutat. Res. 15:1-10.
8. Champlin, F. R., M. L. Ellison, J. W. Bullard, and R. S. Conrad. 2005. Effect of outer membrane permeabilisation on intrinsic resistance to low triclosan levels in Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 26:159-164.
9. Chuanchuen, R., K. Beinlich, T. T. Hoang, A. Becher, R. R. KarkhoffSchweizer, and H. P. Schweizer. 2001. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob. Agents Chemother. 45: 428-432. (Pubitemid 32105276)
10. Chuanchuen, R., R. R. Karkhoff-Schweizer, and H. P. Schweizer. 2003. High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am. J. Infect. Control 31:124-127.
11. Chuanchuen, R., C. T. Narasaki, and H. P. Schweizer. 2002. The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan. J. Bacteriol. 184:5036-5044.
12. Crabbé, A., P. De Boever, R. Van Houdt, H. Moors, M. Mergeay, and P. Cornelis. 2008. Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PAOl. Environ. Microbiol. 10:2098-2110.
13. 2 and poly-beta- hydroxyalkanoate. Biotechnol. Bioeng. 97:279-286.
14. Ellison, M. L., and F. R. Champlin. 2007. Outer membrane permeability for nonpolar antimicrobial agents underlies extreme susceptibility of Pasteurella multocida to the hydrophobic biocide triclosan. Vet. Microbiol. 124:310-318.
15. Favier-Teodorescu, L., J. F. Cornet, and C. G. Dussap. 2003. Modelling continuous culture of Rhodospirillum rubrum in photobioreactor under light limited conditions. Biotechnol. Lett. 25:359-364.
16. Ferenci, T. 2005. Maintaining a healthy SFANC balance through regulatory and mutational adaptation. Mol. Microbiol. 57:1-8.
17. Fernandez, N., E. E. Diaz, R. Amils, and J. L. Sanz. 2008. Analysis of microbial community during biofilm development in an anaerobic wastewater treatment reactor. Microb. Ecol. 56:121-132.
18. George, A. M., and S. B. Levy. 1983. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J. Bacteriol. 155:531-540.
19. Gilbert, P., P. J. Collier, and M. R. Brown. 1990. Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob. Agents Chemother. 34:1865-1868.
20. Heath, R. J., J. R. Rubin, D. R. Holland, E. Zhang, M. E. Snow, and C. O. Rock. 1999. Mechanism of triclosan inhibition of bacterial fatty acid synthesis. J. Biol. Chem. 274:11110-11114.
21. Hendrickx, L., H. De Wever, V. Hermans, F. Mastroleo, N. Morin, A. Wilmotte, P. Janssen, and M. Mergeay. 2006. Microbial ecology of the closed artificial ecosystem MELiSSA (Micro-Ecological Life Support System Alternative): reinventing and compartmentalizing the Earth's food and oxygen regeneration system for long-haul space exploration missions. Res. Microbiol. 157:77-86.
22. Jones, R. D., H. B. Jampani, J. L. Newman, and A. S. Lee. 2000. Triclosan: a review of effectiveness and safety in health care settings. Am. J. Infect. Control 28:184-196.
23. Ledder, R. G., P. Gilbert, C. Willis, and A. J. McBain. 2006. Effects of chronic triclosan exposure upon the antimicrobial susceptibility of 40 ex-situ environmental and human isolates. J. Appl. Microbiol. 100:1132-1140.
24. Lee, I. H., E. J. Kim, Y. H. Cho, and J. K. Lee. 2002. Characterization of a novel enoyl-acyl carrier protein reductase of diazaborine-resistant Rhodobacter sphaeroides mutant. Biochem. Biophys. Res. Commun. 299: 621-627.
25. Levy, S. B. 2002. Active efflux, a common mechanism for biocide and antibiotic resistance. J. Appl. Microbiol. 92(Suppl.):65S-71S.
26. Lomovskaya, O., M. S. Warren, A. Lee, J. Galazzo, R. Fronko, M. Lee, J. Biais, D. Cho, S. Chamberland, T. Renau, R. Leger, S. Hecker, W. Watkins, K. Hoshino, H. Ishida, and V. J. Lee. 2001. Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob. Agents Chemother. 45:105-116.
27. Mailaender, C., N. Reiling, H. Engelhardt, S. Bossmann, S. Ehlers, and M. Niederweis. 2004. The MspA porin promotes growth and increases antibiotic susceptibility of both Mycobacterium bovis BCG and Mycobacterium tuberculosis. Microbiology 150:853-864.
28. McMurry, L. M., P. F. McDermott, and S. B. Levy. 1999. Genetic evidence that InhA oí Mycobacterium smegmatis is a target for triclosan. Antimicrob. Agents Chemother. 43:711-713.
29. McMurry, L. M., M. Oethinger, and S. B. Levy. 1998. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol. Lett. 166:305-309.
30. McMurry, L. M., M. Oethinger, and S. B. Levy. 1998. Triclosan targets lipid synthesis. Nature 394:531-532.
31. Mergeay, M. 1995. Heavy metal resistances in microbial ecosystems, p. 6.1.7.1-6.1.7.17. In A. D. L. Akkermans, J. D. van Elsas, and F. J. De Bruijn (ed.), Molecular microbial ecology manual. Kluwer Academic Press, Dordrecht, Netherlands.
32. Moken, M. C., L. M. McMurry, and S. B. Levy. 1997. Selection of multipleantibiotic-resistant (mar) mutants of Escherichia coli by using the disinfectant pine oil: roles of the mar and acrAB loci. Antimicrob. Agents Chemother. 41:2770-2772.
33. Moore, M. D., and S. Kaplan. 1992. Identification of intrinsic high-level resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria: characterization of tellurite, selenite, and rhodium sesquioxide reduction in Rhodobacter sphaeroides. J. Bacteriol. 174:1505-1514.
34. Ning, C., and H. Gest. 1966. Regulation of L-isoleucine biosynthesis in the photosynthetic bacterium Rhodospirillum rubrum. Proc. Natl. Acad. Sci. U. S. A. 56:1823-1827.
35. Oyaizu, H., H. Kim, D. Honda, I. Takahashi, S. Suzuki, H. Sato, and T. Mino. 2001. Analysis of complex microbial community in soil and wastewater treatment processes by cloning method, p. 336. In T. Matsuo, K. Hanaki, S. Takizawa, and H. Satoh (ed.). Advances in water and wastewater treatment technology: molecular technology, nutrient removal, sludge reduction and environmental health. Elsevier Science BV, Amsterdam, Netherlands.
36. Pycke, B. F. G., G. Vanermen, P. Monsieurs, H. D. Wever, M. Mergeay, W. Verstraete, and N. Leys. Toxicogenomic response of Rhodospirillum rubrum SlH to the micropollutant triclosan. Appl. Environ. Microbiol, in press.
37. Rock, C. O., and J. E. Cronan. 1996. Escherichia coli as a model for the regulation of dissociable (type II) fatty acid biosynthesis. Biochim. Biophys. Acta 1302:1-16.
38. Russell, A. D. 1999. Bacterial resistance to disinfectants: present knowledge and future problems. J. Hosp. Infect. 43(Suppl.):S57-S68.
39. Schweizer, H. P. 1998. Intrinsic resistance to inhibitors of fatty acid biosynthesis in Pseudomonas aeruginosa is due to efflux: application of a novel technique for generation of unmarked chromosomal mutations for the study of efflux systems. Antimicrob. Agents Chemother. 42:394-398.
40. Schweizer, H. P. 2001. Triclosan: a widely used biocide and its link to antibiotics. FEMS Microbiol. Lett. 202:1-7.
41. Sistrom, W. R. 1960. A requirement for sodium in the growth of Rhodopseudomonas spheroides. J. Gen. Microbiol. 22:778-785.
42. Suller, M. T., and A. D. Russell. 2000. Triclosan and antibiotic resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 46:11-18.
43. Tabak, M., K. Scher, E. Hartog, U. Romling, K. R. Matthews, M. L. Chikindas, and S. Yaron. 2007. Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiol. Lett. 267:200-206.
44. Webber, M. A., L. P. Randall, S. Cooles, M. J. Woodward, and L. J. Piddock. 2008. Triclosan resistance in Salmonella enterica serovar Typhimurium. J. Antimicrob. Chemother. 62:83-91.