Characterization of the RND-type multidrug efflux pump MexAB-OprM of the plant pathogen Pseudomonas syringae

Applied and Environmental Microbiology

Volumn 74, Issue 11, 2008, Pages 3387-3393

  Stoitsova, Savina O ^a   Braun, Yvonne ^a   Ullrich, Matthias S ^a   Weingart, Helge ^a  

^a JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; DRUG THERAPY; HEALTH; NUCLEIC ACIDS; PUMPS; RNA; TELLURIUM COMPOUNDS;

AMERICAN SOCIETY; ANTIMICROBIAL COMPOUNDS; DOT-BLOT HYBRIDIZATION; EARLY-EXPONENTIAL PHASE (EEP); GRAM-NEGATIVE BACTERIA; PLANT PATHOGENS; PSEUDOMONAS AERUGINOSA (APRIN); PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. PHASEOLICOLA;

PATHOGENS;

ACRIDINE ORANGE; ACRIFLAVINE; AMPICILLIN; ANTIINFECTIVE AGENT; BACTERIAL RNA; BENZALKONIUM CHLORIDE; BERBERINE; CARBENICILLIN; CEFOPERAZONE; CHLORAMPHENICOL; CIPROFLOXACIN; CLINDAMYCIN; CRYSTAL VIOLET; DAUNORUBICIN; ERYTHROMYCIN; ETHIDIUM BROMIDE; FUSARIC ACID; FUSIDIC ACID; GENTAMICIN; KANAMYCIN; MITOMYCIN C; MULTIDRUG RESISTANCE PROTEIN; NALIDIXIC ACID; NARINGENIN; NITROFURANTOIN; NORFLOXACIN; NOVOBIOCIN; PHLORETIN; PIPERACILLIN; PROTEIN RND;

ANTIMICROBIAL ACTIVITY; BACTERIUM; FRUIT; HYBRIDIZATION; MUTATION; PATHOGEN; RNA;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; DOT HYBRIDIZATION; EFFUSION; GENE MUTATION; NONHUMAN; OPERON; PLANT; PSEUDOMONAS SYRINGAE; TOMATO;

ANTI-BACTERIAL AGENTS; ARABIDOPSIS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ETHIDIUM; GENE DELETION; GENE EXPRESSION PROFILING; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PHASEOLUS; PSEUDOMONAS SYRINGAE;

NEGIBACTERIA; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. PHASEOLICOLA 1448A;

EID: 44949200391     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02866-07     Document Type: Article

References (40)

1. Barabote, R. D., O. L. Johnson, Z. Eric, S. K. San Francisco, J. A. Fralick, and M. J. D. San Francisco. 2003. Erwinia chrysanthemi tolC is involved in resistance to antimicrobial plant chemicals and is essential for phytopathogenesis. J. Bacteriol. 185:5772-5778.
2. Bostock, J. M., G. Huang, S. M. Hashimi, L. Zhang, and R. G. Birch. 2006. A DHA14 drug efflux gene from Xanthomonas albilineans confers high-level albicidin antibiotic resistance in Escherichia coli. J. Appl. Microbiol. 101: 151-160.
3. Buell, C. R., V. Joardar, M. Lindeberg, J. Selengut, I. T. Paulsen, M. L. Gwinn, R. J. Dodson, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, S. Daugherty, L. Brinkac, M. J. Beanan, D. H. Haft, W. C. Nelson, T. Davidsen, N. Zafar, L. Zhou, J. Liu, Q. Yuan, H. Khouri, N. Fedorova, B. Tran, D. Russell, K. Berry, T. Utterback, S. E. Vanaken, T. V. Feldblyum, M. D'Ascenzo, W. L. Deng, A. R. Ramos, J. R. Alfano, S. Cartinhour, A. K. Chatterjee, T. P. Delaney, S. G. Lazarowitz, G. B. Martin, D. J. Schneider, X. Tang, C. L. Bender, O. White, C. M. Fraser, and A. Collmer. 2003. The complete sequence of the tomato and Arabidopsis pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100:10181-10186.
4. Burse, A., H. Weingart, and M. S. Ullrich. 2004. The phytoalexin-inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora. Mol. Plant-Microbe Interact. 17:43-54.
5. Burse, A., H. Weingart, and M. S. Ullrich. 2004. NorM, an Erwinia amylovora multidrug efflux pump involved in in vitro competition with other epiphytic bacteria. Appl. Environ. Microbiol. 70:693-703.
6. Chiou, C. S., and A. L. Jones. 1993. Nucleotide sequence analysis of a transposon (Tn5393) carrying streptomycin resistance genes in Erwinia amylovora and other gram-negative bacteria. J. Bacteriol. 175:732-740.
7. Clinical and Laboratory Standards Institute. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard, 7th ed. CLSI document M7-A7. Clinical and Laboratory Standards Institute, Wayne, PA.
8. Dixon, R. A., and N. L. Paiva. 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085-1097.
9. Evans, K., and K. Poole. 1999. The MexA-MexB-OprM multidrug efflux system of Pseudomonas aeruginosa is growth-phase regulated. FEMS Microbiol. Lett. 173:35-39.
10. Feil, H., W. S. Feil, P. Chain, F. Larimer, G. DiBartolo, A. Copeland, A. Lykidis, S. Trong, M. Nolan, E. Goltsman, J. Thiel, S. Malfatti, J. E. Loper, A. Lapidus, J. C. Detter, M. Land, P. M. Richardson, N. C. Kyrpides, N. Ivanova, and S. E. Lindow. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 102:11064-11069.
11. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
12. Goel, A. K., L. Rajagopal, N. Nagesh, and R. V. Sonti. 2002. Genetic locus encoding functions involved in biosynthesis and outer membrane localization of xanthomonadin in Xanthomonas oryzae pv. oryzae. J. Bacteriol. 184:3539-3548.
13. Gonzáles-Pasayo, R., and E. Martínez-Romero. 2000. Multiresistance genes of Rhizobium etli CFN42. Mol. Plant-Microbe Interact. 13:572-577.
14. Hammerschmidt, R. 1999. Phytoalexins: what have we learned after 60 years? Annu. Rev. Phytopathol. 37:285-306.
15. Hearn, E. M., J. J. Dennis, M. R. Gray, and J. M. Foght. 2003. Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J. Bacteriol. 185:6233-6240.
16. Hirakata, Y., R. Srikumar, K. Poole, N. Gotoh, T. Suematsu, S. Kohno, S. Kamihira, R. E. Hancock, and D. P. Speert. 2002. Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J. Exp. Med. 196:109-118.
17. Hirano, S. S., and C. D. Upper. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae - a pathogen, ice nucleus, and epiphyte. Microbiol. Mol. Biol. Rev. 64:624-653.
18. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
19. Joardar, V., M. Lindeberg, R. W. Jackson, J. Selengut, R. Dodson, L. M. Brinkac, S. C. Daugherty, R. DeBoy, A. S. Durkin, M. G. Giglio, R. Madupu, W. C. Nelson, M. J. Rosovitz, S. Sullivan, J. Crabtree, T. Creasy, T. Davidsen, D. H. Haft, N. Zafar, L. Zhou, R. Halpin, T. Holley, H. Khouri, T. Feldblyum, O. White, C. M. Fraser, A. K. Chatterjee, S. Cartinhour, D. J. Schneider, J. Mansfield, A. Collmer, and C. R. Buell. 2005. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 187:6488-6498.
20. Kang, H., and D. C. Gross. 2005. Characterization of a resistance-nodulation-cell division transporter system associated with the syr-syp genomic island of Pseudomonas syringae pv. syringae. Appl. Environ. Microbiol. 71: 5056-5065.
21. Keane, P. J., A. Kerr, and P. B. New. 1970. Crown gall of stone fruit. II. Identification and nomenclature of Agrobacterium isolates. Aust. J. Biol. Sci. 23:585-595.
22. King, E. O., M. K. Ward, and D. E. Raney. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Clin. Med. 44:301-307.
23. Kumar, A., and H. P. Schweizer. 2005. Bacterial resistance to antibiotics: active efflux and reduced uptake. Adv. Drug Deliv. Rev. 57:1486-1513.
24. Maggiorani Valecillos, A., P. Rodriguez Palenzuela, and E. López-Solanilla. 2006. The role of several multidrug resistance systems in Erwinia chrysantheml pathogenesis. Mol. Plant-Microbe Interact. 19:607-613.
25. Maseda, H., I. Sawada, K. Saito, H. Uchiyama, T. Nakae, and N. Nomura. 2004. Enhancement of the mexAB-oprM efflux pump expression by a quorum-sensing autoinducer and its cancellation by a regulator, MexT, of the mexEF-oprN efflux pump operon in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 48:1320-1328.
26. Ocaktan, A., H. Yoneyama, and T. Nakae. 1997. Use of fluorescence probes to monitor function of the subunit proteins of the MexA-MexB-OprM drug extrusion machinery in Pseudomonas aeruginosa. J. Biol. Chem. 272:21964-21969.
27. Palmer, D. A., and C. L. Bender. 1993. Effects of environmental and nutritional factors on production of the polyketide phytotoxin coronatine by Pseudomonas syringae pv. glycinea. Appl. Environ. Microbiol. 59:1619-1626.
28. Palumbo, J. D., C. I. Kado, and D. A. Phillips. 1998. An isoflavonoid-inducible efflux pump in Agrobacterium tumefaciens is involved in competitive colonization of roots. J. Bacteriol. 180:3107-3113.
29. Paulsen, I. T. 2003. Multidrug efflux pumps and resistance: regulation and evolution. Curr. Opin. Microbiol. 6:446-451.
30. Poole, K. 2004. Efflux-mediated multiresistance in gram-negative bacteria. Qin. Microbiol. Infect. 10:12-26.
31. Poole, K., K. Krebes, C. McNally, and S. Neshat. 1993. Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. J. Bacteriol. 175:7363-7372.
32. Poole, K., K. Tetro, Q. Zhao, S. Neshat, D. E. Heinrichs, and N. Bianco. 1996. Expression of the multidrug resistance operon mexA-mexB-oprM in Pseudomonas aeruginosa: mexR encodes a regulator of operon expression. Antimicrob. Agents Chemother. 40:2021-2028.
33. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Sawada, I., H. Maseda, T. Nakae, H. Uchiyama, and N. Nomura. 2004. A quorum-sensing autoinducer enhances the mexAB-oprM efflux-pump expression without the MexR-mediated regulation in Pseudomonas aeruginosa. Microbiol. Immunol. 48:435-439.
35. Schenk, A., H. Weingart, and M. S. Ullrich. 2008. Extraction of high-quality bacterial RNA from infected leaf tissue for bacterial in planta gene expression analysis by multiplexed fluorescent Northern hybridization. Mol. Plant Pathol. 9:227-235.
36. Tegos, G., F. R. Stermitz, O. Lomovskaya, and K. Lewis. 2002. Multidrug pump inhibitors uncover remarkable activity of plant antimicrobials. Antimicrob. Agents Chemother. 46:3133-3141.
37. Terán, W., A. Felipe, A. Segura, A. Rojas, J.-L. Ramos, and M.-T. Gallegos. 2003. Antibiotic-dependent induction of Pseudomonas putida DOT-TIE TtgABC efflux pump is mediated by the drug binding repressor TtgR. Antimicrob. Agents Chemother. 47:3067-3072.
38. Van Bambeke, F., Y. Glupczynski, P. Plésiat, J. C. Pechère, and P. M. Tulkens. 2003. Antibiotic efflux pumps in prokaryotic cells: occurrence, impact on resistance and strategies for the future of antimicrobial therapy. J. Antimicrob. Chemother. 51:1055-1065.
39. Walsh, C. 2000. Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775-781.
40. Wink, M. 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64:3-19.