1887

Abstract

Benzalkonium chloride (BC) is a commonly used disinfectant and preservative. This study describes changes in expression level at the transcriptomic and proteomic level for K-12 gradually adapted to a tolerance level to BC of 7–8 times the initial MIC. Results from DNA arrays and two-dimensional gel electrophoresis for global gene and protein expression studies were confirmed by real-time quantitative PCR. Peptide mass fingerprinting by MALDI-TOF MS was used to identify differentially expressed proteins. Changes in expression level in adapted cells were shown for porins, drug transporters, glycolytic enzymes, ribosomal subunits and several genes and proteins involved in protection against oxidative stress and antibiotics. Adapted strains showed increased tolerance to several antibiotics. In conclusion, K-12 adapted to higher tolerance to BC acquired several general resistance mechanisms, including responses normally related to the multiple antibiotic resistance (Mar) regulon and protection against oxidative stress. The results revealed that BC treatment might result in superoxide stress in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29288-0
2007-04-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/4/935.html?itemId=/content/journal/micro/10.1099/mic.0.29288-0&mimeType=html&fmt=ahah

References

  1. Aase B., Sundheim G., Langsrud S., Rorvik L. M. 2000; Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes . Int J Food Microbiol 62:57–63 [CrossRef]
    [Google Scholar]
  2. Allen P. N., Noller H. F. 1989; Mutations in ribosomal protein-S4 and protein-S12 influence the higher-order structure of 16-S ribosomal-RNA. J Mol Biol 208:457–468 [CrossRef]
    [Google Scholar]
  3. Almiron M., Link A. J., Furlong D., Kolter R. 1992; A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli . Genes Dev 6:2646–2654 [CrossRef]
    [Google Scholar]
  4. Altuvia S., Almiron M., Huisman G., Kolter R., Storz G. 1994; The Dps promoter is activated by Oxyr during growth and by Ihf and a Sigma(S) in stationary-phase. Mol Microbiol 13:265–272 [CrossRef]
    [Google Scholar]
  5. Azam T. A., Iwata A., Nishimura A., Ueda S., Ishihama A. 1999; Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181:6361–6370
    [Google Scholar]
  6. Barbosa T. M., Levy S. B. 2000; Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA. J Bacteriol 182:3467–3474 [CrossRef]
    [Google Scholar]
  7. Barbosa T. M., Levy S. B. 2002; Activation of the Escherichia coli nfnB gene by MarA through a highly divergent marbox in a class II promoter. Mol Microbiol 45:191–202 [CrossRef]
    [Google Scholar]
  8. Bilgin N., Richter A. A., Ehrenberg M., Dahlberg A. E., Kurland C. G. 1990; Ribosomal-RNA and protein mutants resistant to spectinomycin. EMBO J 9:735–739
    [Google Scholar]
  9. Blattner F. R., Plunkett G., Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K. other authors 1997; The complete genome sequence of Escherichia coli K-12. Science 277:1453–1474 [CrossRef]
    [Google Scholar]
  10. Bohm H., Karch H. 1992; DNA fingerprinting of Escherichia coli O157-H7 strains by pulsed-field gel-electrophoresis. J Clin Microbiol 30:2169–2172
    [Google Scholar]
  11. Bradford M. M. 1976; Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal Biochem 72:248–254 [CrossRef]
    [Google Scholar]
  12. Braoudaki M., Hilton A. C. 2005; Mechanisms of resistance in Salmonella enterica adapted to erythromycin, benzalkonium chloride and triclosan. Int J Antimicrob Agents 25:31–37 [CrossRef]
    [Google Scholar]
  13. Cabiscol E., Tamarit J., Ros J. 2000; Oxidative stress in bacteria and protein damage by reactive oxygen species. Int Microbiol 3:3–8
    [Google Scholar]
  14. Chittum H. S., Champney W. S. 1994; Ribosomal-protein gene sequence changes in erythromycin-resistant mutants of Escherichia coli . J Bacteriol 176:6192–6198
    [Google Scholar]
  15. Choi S. H., Baumler D. J., Kaspar C. W. 2000; Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157 : H7. Appl Environ Microbiol 66:3911–3916 [CrossRef]
    [Google Scholar]
  16. Cohen S. P., Hachler H., Levy S. B. 1993; Genetic and functional analysis of the multiple antibiotic-resistance (Mar) locus in Escherichia coli . J Bacteriol 175:1484–1492
    [Google Scholar]
  17. Compan I., Touati D. 1993; Interaction of six global transcription regulators in expression of manganese superoxide dismutase in Escherichia coli K-12. J Bacteriol 175:1687–1696
    [Google Scholar]
  18. Courcelle J., Khodursky A., Peter B., Brown P. O., Hanawalt P. C. 2001; Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli . Genetics 158:41–64
    [Google Scholar]
  19. Debbasch C., Brignole F., Pisella P. J., Warnet J. M., Rat P., Baudouin C. 2001; Quaternary ammoniums and other preservatives' contribution in oxidative stress and apoptosis on Chang conjunctival cells. Invest Ophthalmol Vis Sci 42:642–652
    [Google Scholar]
  20. Denyer S. P., Maillard J. Y. 2002; Cellular impermeability and uptake of biocides and antibiotics in Gram-negative bacteria. J Appl Microbiol 92:Suppl35S–45S [CrossRef]
    [Google Scholar]
  21. Deshusses J. M. P., Burgess J. A., Scherl A., Wenger Y., Walter N., Converset V., Paesano S., Corthals G. L., Hochstrasser D. F., Sanchez J. C. 2003; Exploitation of specific properties of trifluoroethanol for extraction and separation of membrane proteins. Proteomics 3:1418–1424 [CrossRef]
    [Google Scholar]
  22. Eisenman H. C., Craig E. A. 2004; Activation of pleiotropic drug resistance by the J-protein and Hsp70-related proteins, Zuo1 and Ssz1. Mol Microbiol 53:335–344 [CrossRef]
    [Google Scholar]
  23. Folio P., Chavant P., Chafsey I., Belkorchia A., Chambon C., Hébraud M. 2004; Two-dimensional electrophoresis database of Listeria monocytogenes EGDe proteome and proteomic analysis of mid-log and stationary growth phase cells. Proteomics 4:3187–3201 [CrossRef]
    [Google Scholar]
  24. Funatsu G., Wittmann H. G., Schiltz E. 1972; Ribosomal-proteins. 27. Localization of amino-acid exchanges in protein S5 from two Escherichia coli mutants resistant to spectinomycin. Mol Gen Genet 114:106–111 [CrossRef]
    [Google Scholar]
  25. Gilbert P., Moore L. E. 2005; Cationic antiseptics: diversity of action under a common epithet. J Appl Microbiol 99:703–715 [CrossRef]
    [Google Scholar]
  26. Greenberg J. T., Monach P., Chou J. H., Josephy P. D., Demple B. 1990; Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli . Proc Natl Acad Sci U S A 87:6181–6185 [CrossRef]
    [Google Scholar]
  27. Heir E., Sundheim G., Holck A. L. 1995; Resistance to quaternary ammonium compounds in Staphylococcus spp. isolated from the food industry and nucleotide sequence of the resistance plasmid pST827. J Appl Microbiol 79:149–156
    [Google Scholar]
  28. Heir E., Sundheim G., Holck A. L. 1999; The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J Appl Microbiol 86:378–388 [CrossRef]
    [Google Scholar]
  29. Ishikawa S., Matsumura Y., Yoshizako F., Tsuchido T. 2002; Characterization of a cationic surfactant-resistant mutant isolated spontaneously from Escherichia coli . J Appl Microbiol 92:261–268 [CrossRef]
    [Google Scholar]
  30. Kang W. K., Icho T., Isono S., Kitakawa M., Isono K. 1989; Characterization of the gene rimk responsible for the addition of glutamic-acid residues to the C-terminus of ribosomal protein-S6 in Escherichia coli K12. Mol Gen Genet 217:281–288 [CrossRef]
    [Google Scholar]
  31. Khil P. P., Camerini-Otero R. D. 2002; Over 1000 genes are involved in the DNA damage response of Escherichia coli . Mol Microbiol 44:89–105 [CrossRef]
    [Google Scholar]
  32. Kirkpatrick C., Maurer L. M., Oyelakin N. E., Yoncheva Y. N., Maurer R., Slonczewski J. L. 2001; Acetate and formate stress: opposite responses in the proteome of Escherichia coli . J Bacteriol 183:6466–6477 [CrossRef]
    [Google Scholar]
  33. Langsrud Ø. 2002; 50-50 multivariate analysis of variance for collinear responses. J R Stat Soc Ser D 51:305–317 [CrossRef]
    [Google Scholar]
  34. Langsrud Ø. 2005; Rotation tests. Stat Comput 15:53–60 [CrossRef]
    [Google Scholar]
  35. Langsrud S., Sundheim G., Borgmann-Strahsen R. 2003; Intrinsic and acquired resistance to quaternary ammonium compounds in food-related Pseudomonas spp. J Appl Microbiol 95:874–882 [CrossRef]
    [Google Scholar]
  36. Langsrud S., Sundheim G., Holck A. L. 2004; Cross-resistance to antibiotics of Escherichia coli adapted to benzalkonium chloride or exposed to stress-inducers. J Appl Microbiol 96:201–208 [CrossRef]
    [Google Scholar]
  37. Len A. C. L., Harty D. W. S., Jacques N. A. 2004; Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance. Microbiology 150:1339–1351 [CrossRef]
    [Google Scholar]
  38. Li X. Z., Nikaido H. 2004; Efflux-mediated drug resistance in bacteria. Drugs 64:159–204 [CrossRef]
    [Google Scholar]
  39. Liochev S. I., Fridovich I. 1992; Fumarase-C, the stable fumarase of Escherichia coli , is controlled by the SoxRS regulon. Proc Natl Acad Sci U S A 89:5892–5896 [CrossRef]
    [Google Scholar]
  40. Lomovskaya O. L., Kidwell J. P., Matin A. 1994; Characterization of the sigma(38)-dependent expression of a core Escherichia coli starvation gene, pexb . J Bacteriol 176:3928–3935
    [Google Scholar]
  41. Ma D., Cook D. N., Alberti M., Pon N. G., Nikaido H., Hearst J. E. 1995; Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli . Mol Microbiol 16:45–55 [CrossRef]
    [Google Scholar]
  42. Majtan V., Majtanova L., Hostacka A., Hybenova D., Mlynarcik D. 1995; Effect of quaternary ammonium salts and amine oxides on Pseudomonas aeruginosa . Microbios 84:41–51
    [Google Scholar]
  43. Martin R. G., Gillette W. K., Rosner J. L. 2000; Promoter discrimination by the related transcriptional activators MarA and SoxS: differential regulation by differential binding. Mol Microbiol 35:623–634
    [Google Scholar]
  44. Martinez A., Kolter R. 1997; Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179:5188–5194
    [Google Scholar]
  45. Martinez-Martinez L., Conejo M. C., Pascual A., Hernandez-Alles S., Ballesta S., De Arellano-Ramos E. R., Benedi V. J., Perea E. J. 2000; Activities of imipenem and cephalosporins against clonally related strains of Escherichia coli hyperproducing chromosomal beta-lactamase and showing altered porin profiles. Antimicrob Agents Chemother 44:2534–2536 [CrossRef]
    [Google Scholar]
  46. Maurer L. M., Yohannes E., Bondurant S. S., Radmacher M., Slonczewski J. L. 2005; pH regulates genes for flagellar motility, catabolism, and oxidative stress in Escherichia coli K-12. J Bacteriol 187:304–319 [CrossRef]
    [Google Scholar]
  47. McDonnell G., Russell A. D. 1999; Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179
    [Google Scholar]
  48. McMurry L. M., Oethinger M., Levy S. B. 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 [CrossRef]
    [Google Scholar]
  49. Moen B., Oust A., Langsrud O., Dorrell N., Marsden G. L., Hinds J., Kohler A., Wren B. W., Rudi K. 2005; Explorative multifactor approach for investigating global survival mechanisms of Campylobacter jejuni under environmental conditions. Appl Environ Microbiol 71:2086–2094 [CrossRef]
    [Google Scholar]
  50. Moken M. C., McMurry L. M., Levy S. B. 1997; Selection of multiple-antibiotic-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
    [Google Scholar]
  51. Molloy M. P., Herbert B. R., Williams K. L., Gooley A. A. 1999; Extraction of Escherichia coli proteins with organic solvents prior to two-dimensional electrophoresis. Electrophoresis 20:701–704 [CrossRef]
    [Google Scholar]
  52. Nair S., Finkel S. E. 2004; Dps protects cells against multiple stresses during stationary phase. J Bacteriol 186:4192–4198 [CrossRef]
    [Google Scholar]
  53. NCCLS 2002 Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow AerobicallyNCCLS approved standard M7-A5 Wayne, PA: National Committee for Clinical Laboratory Standards;
    [Google Scholar]
  54. Nestorovich E. M., Danelon C., Winterhalter M., Bezrukov S. M. 2002; Designed to penetrate: time-resolved interaction of single antibiotic molecules with bacterial pores. Proc Natl Acad Sci U S A 99:9789–9794 [CrossRef]
    [Google Scholar]
  55. Neuhoff V., Arold N., Taube D., Ehrhardt W. 1988; Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262 [CrossRef]
    [Google Scholar]
  56. Nikaido H. 2001; Preventing drug access to targets: cell surface permeability barriers and active efflux in bacteria. Semin Cell Dev Biol 12:215–223 [CrossRef]
    [Google Scholar]
  57. Nishino K., Yamaguchi A. 2004; Role of histone-like protein H-NS in multidrug resistance of Escherichia coli . J Bacteriol 186:1423–1429 [CrossRef]
    [Google Scholar]
  58. Nunoshiba T., Hidalgo E., Amabile Cuevas C. F., Demple B. 1992; Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene. J Bacteriol 174:6054–6060
    [Google Scholar]
  59. Paterson E. S., Boucher S. E., Lambert I. B. 2002; Regulation of the nfsA gene in Escherichia coli by SoxS. J Bacteriol 184:51–58 [CrossRef]
    [Google Scholar]
  60. Petersen A., Aarestrup F. M., Hofshagen M., Franklin A., Gunnarsson E., Sipulä H. 2003; Harmonization of antimicrobial susceptibility testing among veterinary diagnostic laboratories in the five Nordic countries. Microbial Drug Resist 9:381–388 [CrossRef]
    [Google Scholar]
  61. Pomposiello P. J., Bennik M. H., Demple B. 2001; Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183:3890–3902 [CrossRef]
    [Google Scholar]
  62. Poole K. 2004; Efflux-mediated multiresistance in Gram-negative bacteria. Clin Microbiol Infect 10:12–26
    [Google Scholar]
  63. Poole K. 2005; Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 56:20–51 [CrossRef]
    [Google Scholar]
  64. Rabilloud T., Brodard V., Peltre G., Righetti P. G., Ettori C. 1992; Modified silver staining for immobilized pH gradients. Electrophoresis 13:264–266 [CrossRef]
    [Google Scholar]
  65. Randall L. P., Woodward M. J. 2002; The multiple antibiotic resistance ( mar ) locus and its significance. Res Vet Sci 72:87–93 [CrossRef]
    [Google Scholar]
  66. Rudi K., Nogva H. K., Naterstad K., Dromtorp S. M., Bredholt S., Holck A. 2003; Subtyping Listeria monocytogenes through the combined analyses of genotype and expression of the hlyA virulence determinant. J Appl Microbiol 94:720–732 [CrossRef]
    [Google Scholar]
  67. Sakagami Y., Yokoyama H., Nishimura H., Ose Y., Tashima T. 1989; Mechanism of resistance to benzalkonium chloride by Pseudomonas aeruginosa . Appl Environ Microbiol 55:2036–2040
    [Google Scholar]
  68. Soumet C., Ragimbeau C., Maris P. 2005; Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production. Lett Appl Microbiol 41:291–296 [CrossRef]
    [Google Scholar]
  69. Steinman H. M., Weinstein L. 1993; Manganese superoxide-dismutase of Escherichia coli binds DNA – Escherichia coli FeSod does not – implications for in-vivo function. Free Radic Biol Med 15:476
    [Google Scholar]
  70. Steinman H. M., Weinstein L., Brenowitz M. 1994; The manganese superoxide-dismutase of Escherichia coli K-12 associates with DNA. J Biol Chem 269:28629–28634
    [Google Scholar]
  71. Tavio M. D., Vila J., Ruiz J., Martin-Sanchez A. M., de Anta M. T. J. 1999; Mechanisms involved in the development of resistance to fluoroquinolones in Escherichia coli isolates. J Antimicrob Chemother 44:735–742 [CrossRef]
    [Google Scholar]
  72. Tikhonova E. B., Zgurskaya H. I. 2004; AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. J Biol Chem 279:32116–32124 [CrossRef]
    [Google Scholar]
  73. Tseng C. P., Yu C. C., Lin H. H., Chang C. Y., Kuo J. T. 2001; Oxygen- and growth rate-dependent regulation of Escherichia coli fumarase (FumA, FumB, and FumC) activity. J Bacteriol 183:461–467 [CrossRef]
    [Google Scholar]
  74. van Schie B. J., Hellingwerf K. J., Elferink M. G., Kuenen J. G., Konings W. N., van Dijken J. P., van Dijl J. M. 1985; Energy transduction by electron transfer via a pyrrolo-quinoline quinone-dependent glucose dehydrogenase in Escherichia coli , Pseudomonas aeruginosa , and Acinetobacter calcoaceticus (var. lwoffi ). J Bacteriol 163:493–499
    [Google Scholar]
  75. Wang G., Maier R. J. 2004; An NADPH quinone reductase of Helicobacter pylori plays an important role in oxidative stress resistance and host colonization. Infect Immun 72:1391–1396 [CrossRef]
    [Google Scholar]
  76. Wilcox S. K., Cavey G. S., Pearson J. D. 2001; Single ribosomal protein mutations in antibiotic-resistant bacteria analyzed by mass spectrometry. Antimicrob Agents Chemother 45:3046–3055 [CrossRef]
    [Google Scholar]
  77. Witte G., Urbanke C., Curth U. 2003; DNA polymerase III chi subunit ties single-stranded DNA binding protein to the bacterial replication machinery. Nucleic Acids Res 31:4434–4440 [CrossRef]
    [Google Scholar]
  78. Wolf S. G., Frenkiel D., Arad T., Finkel S. E., Kolter R., Minsky A. 1999; DNA protection by stress-induced biocrystallization. Nature 400:83–85 [CrossRef]
    [Google Scholar]
  79. Wright N. E., Gilbert P. 1987; Antimicrobial activity of n-alkyltrimethylammonium bromides: influence of specific growth rate and nutrient limitation. J Pharm Pharmacol 39:685–690 [CrossRef]
    [Google Scholar]
  80. Wu J., Weiss B. 1992; Two-stage induction of the soxRS (superoxide response) regulon of Escherichia coli . J Bacteriol 174:3915–3920
    [Google Scholar]
  81. Yamada M., Asaoka S., Yamada Y., Saier M. H. Jr 1993a; Characterization of the gcd gene from Escherichia coli K-12 W3110 and regulation of its expression. J Bacteriol 175:568–571
    [Google Scholar]
  82. Yamada M., Sumi K., Matsushita K., Adachi O., Yamada Y. 1993b; Topological analysis of quinoprotein glucose dehydrogenase in Escherichia coli and its ubiquinone-binding site. J Biol Chem 268:12812–12817
    [Google Scholar]
  83. Zgurskaya H. I., Nikaido H. 2000; Cross-linked complex between oligomeric periplasmic lipoprotein AcrA and the inner-membrane-associated multidrug efflux pump AcrB from Escherichia coli . J Bacteriol 182:4264–4267 [CrossRef]
    [Google Scholar]
  84. Zheng M., Wang X., Templeton L. J., Smulski D. R., LaRossa R. A., Storz G. 2001; DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29288-0
Loading
/content/journal/micro/10.1099/mic.0.29288-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error