Identification and characterization of a novel multidrug resistance operon, mdtRP (yusOP), of Bacillus subtilis

Journal of Bacteriology

Volumn 191, Issue 10, 2009, Pages 3273-3281

  Kim, Ji Yun ^a,b   Inaoka, Takashi ^a   Hirooka, Kazutaka ^c   Matsuoka, Hiroshi ^c   Murata, Makiko ^d   Ohki, Reiko ^d   Adachi, Yoshikazu ^b   Fujita, Yasutaro ^c   Ochi, Kozo ^a  

^a NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

^b IBARAKI UNIVERSITY   (Japan)

^c FUKUYAMA UNIVERSITY   (Japan)

^d KYORIN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ARGININE; BACTERIAL DNA; DACTINOMYCIN; DEOXYRIBONUCLEASE I; FUSIDIC ACID; LYSINE; NOVOBIOCIN; STREPTOMYCIN; THREONINE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BINDING AFFINITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA FOOTPRINTING; GEL MOBILITY SHIFT ASSAY; GENE DISRUPTION; GENE EXPRESSION; GENE IDENTIFICATION; GENE REPRESSION; GENETIC TRANSCRIPTION; MDTRP GENE; MULTIDRUG RESISTANCE; MUTANT; MUTATION; NONHUMAN; NORTHERN BLOTTING; OPERON; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; SEQUENCE ANALYSIS; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

BACILLUS SUBTILIS;

ANTI-BACTERIAL AGENTS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BLOTTING, NORTHERN; DACTINOMYCIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FUSIDIC ACID; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; NOVOBIOCIN; OPERON; PROTEIN BINDING; STREPTOMYCIN;

EID: 65549102913     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00151-09     Document Type: Article

References (37)

1. Albert, T. J., D. Dailidiene, G. Dailide, J. E. Norton, A. Kalia, T. A. Richmond, M. Molla, J. Singh, R. D. Green, and D. E. Berg. 2005. Mutation discovery in bacterial genomes: metronidazole resistance in Helicobacter pylori. Nat. Methods 2:951-953.
2. Alekshun, M. N., Y. S. Kim, and S. B. Levy. 2000. Mutational analysis of MarR, the negative regulator of marRAB expression in Escherichia coli, suggests the presence of two regions required for DNA binding. Mol. Microbiol. 35:1394-1404.
3. Alekshun, M. N., S. B. Levy, T. R. Mealy, B. A. Seaton, and J. F. Head. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 Å resolution. Nat. Struct. Biol. 8:710-714.
4. Besier, S., A. Ludwig, V. Brade, and T. A. Wichelhaus. 2003. Molecular analysis of fusidic acid resistance in Staphylococcus aureus. Mol. Microbiol. 47:463-469.
5. Bodley, J. W., F. J. Zieve, L. Lin, and S. T. Zieve. 1969. Formation of the ribosome-G factor-GDP complex in the presence of fusidic acid. Biochem. Biophys. Res. Commun. 37:437-443.
6. Dzidic, S., J. Suskovic, and B. Kos. 2008. Antibiotic resistance mechanisms in bacteria: biochemical and genetic aspects. Food Technol. Biotechnol. 46:11-21.
7. Fujita, Y., and Y. Miwa. 1989. Identification of an operator sequence for the Bacillus subtilis gnt operon. J. Biol. Chem. 264:4201-4206.
8. Furukawa, H., J. T. Tsay, S. Jackowski, Y. Takamura, and C. O. Rock. 1993. Thiolactomycin resistance in Escherichia coli is associated with the multidrug resistance efflux pump encoded by emrAB. J. Bacteriol. 175:3723-3729. (Pubitemid 23173332)
9. Haldenwang, W. G. 1995. The sigma factors of Bacillus subtilis. Microbiol. Rev. 59:1-30.
10. Hirooka, K., S. Kunikane, H. Matsuoka, K. Yoshida, K. Kumamoto, S. Tojo, and Y. Fujita. 2007. Dual regulation of the Bacillus subtilis regulon comprising the lmrAB and yxaGH operons and yxaF gene by two transcriptional repressors, LarA and YxaF, in response to flavonoids. J. Bacteriol. 189:5170-5182.
11. Hosaka, T., N. Tamehiro, N. Chumpolkulwong, C. Hori-Takemoto, M. Shirouzu, S. Yokoyama, and K. Ochi. 2004. The novel mutation K87E in ribosomal protein S12 enhances protein synthesis activity during the late growth phase in Escherichia coli. Mol. Genet. Genomics 271:317-324. (Pubitemid 38591179)
12. Hosaka, T., J. Xu, and K. Ochi. 2006. Increased expression of ribosome recycling factor is responsible for the enhanced protein synthesis during the late growth phase in an antibiotic-overproducing Streptomyces coelicolor ribosomal rpsL mutant. Mol. Microbiol. 61:883-897. (Pubitemid 44134168)
13. Inaoka, T., K. Kasai, and K. Ochi. 2001. Construction of an in vivo nonsense readthrough assay system and functional analysis of ribosomal proteins S12, S4, and S5 in Bacillus subtilis. J. Bacteriol. 183:4958-4963. (Pubitemid 32750921)
14. Inaoka, T., and K. Ochi. 2007. Regulation of secondary metabolism in Bacillus subtilis, p. 143-154. In Y. Fujita (ed.), Global regulatory networks in Bacillus subtilis. Transworld Research Network, Kerala, India.
15. Inaoka, T., K. Takahashi, M. Ohnishi-Kameyama, M. Yoshida, and K. Ochi. 2003. Guanine nucleotides guanosine 5′-diphosphate 3′-diphosphate and GTP co-operatively regulate the production of an antibiotic bacilysin in Bacillus subtilis. J. Biol. Chem. 278:2169-2176. (Pubitemid 36801282)
16. Inaoka, T., K. Takahashi, H. Yada, M. Yoshida, and K. Ochi. 2004. RNA polymerase mutation activates the production of a dormant antibiotic 3,3′-neotrehalosadiamine via an autoinduction mechanism in Bacillus subtilis. J. Biol. Chem. 279:3885-3892. (Pubitemid 38140634)
17. Inaoka, T., T. Satomura, Y. Fujita, and K. Ochi. 2009. Novel gene regulation mediated by overproduction of secondary metabolite neotrehalosadiamine in Bacillus subtilis. FEMS Microbiol. Lett. 291:151-156.
18. Kobayashi, H., K. Kobayashi, and Y. Kobayashi. 1977. Isolation and characterization of fusidic acid-resistant, sporulation-defective mutants of Bacillus subtilis. J. Bacteriol. 132:262-269. (Pubitemid 8194545)
19. Kobayashi, K., S. D. Ehrlich, A. Albertini, G. Amati, K. K. Andersen, M. Arnaud, K. Asai, S. Ashikaga, S. Aymerich, P. Bessieres, F. Boland, S. C. Brignell, S. Bron, K. Bunai, J. Chapuis, L. C. Christiansen, A. Danchin, M. Debarbouille, E. Dervyn, E. Deuerling, K. Devine, S. K. Devine, O. Dreesen, J. Errington, S. Fillinger, S. J. Foster, Y. Fujita, A. Galizzi, R. Gardan, C. Eschevins, T. Fukushima, K. Haga, C. R. Harwood, M. Hecker, D. Hosoya, M. F. Hullo, H. Kakeshita, D. Karamata, Y. Kasahara, F. Kawamura, K. Koga, P. Koski, R. Kuwana, D. Imamura, M. Ishimaru, S. Ishikawa, I. Ishio, D. Le Coq, A. Masson, C. Mauel, R. Meima, R. P. Mellado, A. Moir, S. Moriya, E. Nagakawa, H. Nanamiya, S. Nakai, P. Nygaard, M. Ogura, T. Ohanan, M. O'Reilly, M. O'Rourke, Z. Pragai, H. M. Pooley, G. Rapoport, J. P. Rawlins, L. A. Rivas, C. Rivolta, A. Sadaie, Y. Sadaie, M. Sarvas, T. Sato, H. H. Saxild, E. Scanlan, W. Schumann, J. F. Seegers, J. Sekiguchi, A. Sekowska, S. J. Seror, M. Simon, P. Stragier, R. Studer, H. Takamatsu, T. Tanaka, M. Takeuchi, H. B. Thomaides, V. Vagner, J. M. van Dijl, K. Watabe, A. Wipat, H. Yamamoto, M. Yamamoto, Y. Yamamoto, K. Yamane, K. Yata, K. Yoshida, H. Yoshikawa, U. Zuber, and N. Ogasawara. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-4683.
20. Kurosawa, K., T. Hosaka, N. Tamehiro, T. Inaoka, and K. Ochi. 2006. Improvement of α-amylase production by modulation of ribosomal component protein S12 in Bacillus subtilis 168. Appl. Environ. Microbiol. 72:71-77.
21. Laurberg, M., O. Kristensen, K. Martemyanov, A. T. Gudkov, I. Nagaev, D. Hughes, and A. Liljas. 2000. Structure of a mutant EF-G reveals domain III and possibly the fusidic acid binding site. J. Mol. Biol. 303:593-603.
22. Littlejohn, T. G., I. T. Paulsen, M. T. Gillespie, J. M. Tennent, M. Midgley, I. G. Jones, A. S. Purewal, and R. A. Skurray. 1992. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol. Lett. 95:259-266.
23. Lomovskaya, O., and K. Lewis. 1992. emr, an Escherichia coli locus for multidrug resistance. Proc. Natl. Acad. Sci. USA 89:8938-8942.
24. Moriya, S., E. Tsujikawa, A. K. Hassan, K. Asai, T. Kodama, and N. Ogasawara. 1998. A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol. Microbiol. 29:179-187.
25. Nishimura, K., T. Hosaka, S. Tokuyama, S. Okamoto, and K. Ochi. 2007. Mutations in rsmG, encoding a 16S rRNA methyltransferase, result in lowlevel streptomycin resistance and antibiotic overproduction in Streptomyces coelicolor A3(2). J. Bacteriol. 189:3876-3883. (Pubitemid 46740185)
26. Nishimura, K., S. K. Johansen, T. Inaoka, T. Hosaka, S. Tokuyama, Y. Tahara, S. Okamoto, F. Kawamura, S. Douthwaite, and K. Ochi. 2007. Identification of the RsmG methyltransferase target as 16S rRNA nucleotide G527 and characterization of Bacillus subtilis rsmG mutants. J. Bacteriol. 189:6068-6073.
27. Ochi, K. 2007. From microbial differentiation to ribosome engineering. Biosci. Biotechnol. Biochem. 71:1373-1386.
28. Ochi, K., S. Okamoto, Y. Tozawa, T. Inaoka, T. Hosaka, J. Xu, and K. Kurosawa. 2004. Ribosome engineering and secondary metabolite production. Adv. Appl. Microbiol. 56:155-184.
29. Ochi, K., J. Y. Kim, Y. Tanaka, G. Wang, K. Masuda, H. Nanamiya, S. Okamoto, S. Tokuyama, Y. Adachi, and F. Kawamura. 2009. Inactivation of KsgA, a 16S rRNA methyltransferase, causes vigorous emergence of mutants with high-level kasugamycin resistance. Antimicrob. Agents Chemother. 53:193-201.
30. Okamoto, S., A. Tamaru, C. Nakajima, K. Nishimura, Y. Tanaka, S. Tokuyama, Y. Suzuki, and K. Ochi. 2007. Loss of a conserved 7-methylguanosine modification in 16S rRNA confers low-level streptomycin resistance in bacteria. Mol. Microbiol. 63:1096-1106.
31. Okamoto-Hosoya, Y., T. Hosaka, and K. Ochi. 2003. An aberrant protein synthesis activity is linked with antibiotic overproduction in rpsL mutants of Streptomyces coelicolor A3(2). Microbiology 149:3299-3309.
32. Satomura, T., D. Shimura, K. Asai, Y. Sadaie, K. Hirooka, and Y. Fujita. 2005. Enhancement of glutamine utilization in Bacillus subtilis through the GlnK-GlnL two-component regulatory system. J. Bacteriol. 187:4813-4821.
33. Tamehiro, N., T. Hosaka, J. Xu, H. Hu, N. Otake, and K. Ochi. 2003. Innovative approach for improvement of an antibiotic-overproducing industrial strain of Streptomyces albus. Appl. Environ. Microbiol. 69:6412-6417. (Pubitemid 37420171)
34. Vagner, V., E. Dervyn, and S. D. Ehrlich. 1998. A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144:3097-3104.
35. Walsh, C. 2000. Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775-781.
36. Wang, G., T. Hosaka, and K. Ochi. 2008. Dramatic activation of antibiotic production in Streptomyces coelicolor by cumulative drug resistance mutations. Appl. Environ. Microbiol. 74:2834-2840.
37. Yoshida, K., K. Kobayashi, Y. Miwa, C. M. Kang, M. Matsunaga, H. Yamaguchi, S. Tojo, M. Yamamoto, R. Nishi, N. Ogasawara, T. Nakayama, and Y. Fujita. 2001. Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. Nucleic Acids Res. 29:683-692. (Pubitemid 32124379)