A novel insertion mutation in Streptomyces coelicolor ribosomal S12 protein results in paromomycin resistance and antibiotic overproduction

Antimicrobial Agents and Chemotherapy

Volumn 53, Issue 3, 2009, Pages 1019-1026

  Wang, Guojun ^a   Inaoka, Takashi ^a   Okamoto, Susumu ^a   Ochi, Kozo ^a  

^a NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINORHODINE; GLYCINE; PAROMOMYCIN; PRODIGIOSIN; RNA 12S; UNCLASSIFIED DRUG; UNDECYLPRODIGIOSIN;

ACTII REGULATOR GENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DRUG MANUFACTURE; ESCHERICHIA COLI; GENE INSERTION; GENE MUTATION; GROWTH CURVE; ORF4 REGULATOR GENE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATOR GENE; RIBOSOME; RNA TRANSLATION; RPSL BACTERIAL GENE; STREPTOMYCES COELICOLOR; TRANSCRIPTION INITIATION;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; CELL-FREE SYSTEM; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GLYCINE; GREEN FLUORESCENT PROTEINS; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; MUTAGENESIS, INSERTIONAL; PAROMOMYCIN; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RNA, BACTERIAL; SEQUENCE ANALYSIS, DNA; STREPTOMYCES COELICOLOR;

EID: 62949152302     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00388-08     Document Type: Article

References (43)

1. Carr, J. F., S. T. Gregory, and A. E. Dahlberg. 2005. Severity of the streptomycin resistance and streptomycin dependence phenotypes of ribosomal protein S12 of Thermus thermophilus depends on the identity of highly conserved amino acid residues. J. Bacteriol. 187:3548-3550.
2. Carter, A. P., W. M. Clemons, D. E. Brodersen, R. J. Morgan-Warren, B. T. Wimberly, and V. Ramakrishnan. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407:340-348.
3. Fourmy, D., M. I. Recht, S. C. Blanchard, and J. D. Puglisi. 1996. Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274:1367-1371.
4. Gramajo, H. C., E. Takano, and M. J. Bibb. 1993. Stationary-phase production of the antibiotic actinorhodin in Streptomyces coelicolor A3(2) is transcriptionally regulated. Mol. Microbiol. 7:837-845.
5. Green, R., and H. F. Noller. 1997. Ribosomes and translation. Annu. Rev. Biochem. 66:679-716.
6. Gromadski, K. B., and M. V. Rodnina. 2004. Streptomycin interferes with conformational coupling between codon recognition and GTPase activation on the ribosome. Nat. Struct. Mol. Biol. 11:316-322.
7. Hesketh, A., and K. Ochi. 1997. A novel method for improving Streptomyces coelicolor A3(2) for production of actinorhodin by introduction of rpsL (encoding ribosomal protein S12) mutations conferring resistance to streptomycin. J. Antibiot. (Tokyo) 50:532-535.
8. Hirokawa, G., H. Kaji, and A. Kaji. 2007. Inhibition of antiassociation activity of translation initiation factor 3 by paromomycin. Antimicrob. Agents Chemother. 51:175-180.
9. Hobbie, S. N., P. Pfister, C. Bruell, P. Sander, B. Francois, E. Westhof, and E. C. Bottger. 2006. Binding of neomycin-class aminoglycoside antibiotics to mutant ribosomes with alterations in the A site of 16S rRNA. Antimicrob. Agents Chemother. 50:1489-1496.
10. 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.
11. 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.
12. Hosokawa, K., N. H. Park, T. Inaoka, Y. Itoh, and K. Ochi. 2002. Streptomycin-resistant (rpsL) or rifampicin-resistant (rpoB) mutation in Pseudomonas putida KH146-2 confers enhanced tolerance to organic chemicals. Environ. Microbiol. 4:703-712.
13. Hosoya, Y., S. Okamoto, H. Muramatsu, and K. Ochi. 1998. Acquisition of certain streptomycin-resistant (str) mutations enhances antibiotic production in bacteria. Antimicrob. Agents Chemother. 42:2041-2047.
14. Hu, H., and K. Ochi. 2001. Novel approach for improving the productivity of antibiotic-producing strains by inducing combined resistant mutations. Appl. Environ. Microbiol. 67:1885-1892.
15. 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.
16. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
17. 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.
18. Li, M., A. Tzagoloff, K. Underbrink-Lyon, and N. C. Martin. 1982. Identification of the paromomycin-resistance mutation in the 15S rRNA gene of yeast mitochondria. J. Biol. Chem. 25:5921-5928.
19. Lodmell, J. S., and A. E. Dahlberg. 1997. A conformational switch in Escherichia coli 16S ribosomal RNA during decoding of messenger RNA. Science 277:1262-1267.
20. Momose, H., and L. Gorini. 1971. Genetic analysis of streptomycin dependence in Escherichia coli. Genetics 67:19-38.
21. Nishimura, K., T. Hosaka, S. Tokuyama, S. Okamoto, and K. Ochi. 2007. Mutations in rsmG, encoding a 16S rRNA methyltranferase, result in low-level streptomycin resistance and antibiotic overproduction in Streptomyces coelicolorA3(2). J. Bacteriol. 189:3876-3883.
22. Nomura, M. 1970. Bacterial ribosome. Bacteriol. Rev. 34:228-277.
23. Ochi, K. 2007. From microbial differentiation to ribosome engineering. Biosci. Biotechnol. Biochem. 71:1373-1386.
24. 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.
25. Ogle, J. M., F. V. Murphy, M. J. Tarry, and V. Ramakrishnan. 2002. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111:721-732.
26. Okamoto-Hosoya, Y., T. Sato, and K. Ochi. 2000. Resistance to paromomycin is conferred by rpsL mutations, accompanied by an enhanced antibiotic production in Streptomyces coelicolor A3(2). J. Antibiot. (Tokyo) 53:1424-1427.
27. 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.
28. 2-terminal acetylation. Methods Enzymol. 96:150-157.
29. Peske, F., A. Savelsbergh, V. I. Katunin, M. V. Rodnina, and W. Wintermeyer. 2004. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J. Mol. Biol. 343:1183-1194.
30. Pfister, P., S. Hobbie, Q. Vicens, E. C. Bottger, and E. Westhof. 2003. The molecular basis for A-site mutations conferring aminoglycoside resistance: relationship between ribosomal susceptibility and X-ray crystal structures. Chembiochem 4:1078-1088.
31. Recht, M. I., S. Douthwaite, K. D. Dahlquist, and J. D. Puglisi. 1999. Effect of mutations in the A site of 16S rRNA on aminoglycoside antibiotic-ribosome interaction. J. Mol. Biol. 286:33-43.
32. Sharma, D., A. R. Cukras, E. J. Rogers, D. R. Southworth, and R. Green. 2007. Mutational analysis of S12 protein and implications for the accuracy of decoding by the ribosome. J. Mol. Biol. 374:1065-1076.
33. Shima, J., A. Hesketh, S. Okamoto, S. Kawamoto, and K. Ochi. 1996. Induction of actinorhodin production by rpsL (encoding ribosomal protein S12) mutations that confer streptomycin resistance in Streptomyces lividans and Streptomyces coelicolor A3(2). J. Bacteriol. 178:7276-7284.
34. Spangler, E. A., and E. H. Blackburn. 1985. The nucleotide sequence of the 17S ribosomal RNA gene of Tetrahymena thermophila and the identification of point mutations resulting in resistance to the antibiotics paromomycin and hygromycin. J. Biol. Chem. 260:6334-6340.
35. 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.
36. Tenson, T., and A. Mankin. 2006. Antibiotics and the ribosome. Mol. Microbiol. 59:1664-1677.
37. Vicens, Q., and E. Westhof. 2001. Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure 9:647-658.
38. 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.
39. Wilson, D. N. 2004. Antibiotics and the inhibition of ribosome function, p. 449-527. In D. N. Wilson and K. H. Nierhaus (ed.), Protein synthesis and ribosome structure: translating the genome. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany.
40. Wirmer, J., and E. Westhof. 2006. Molecular contacts between antibiotics and the 30S ribosomal particle. Methods Enzymol. 415:180-202.
41. Xu, J., Y. Tozawa, C. Lai, H. Hayashi, and K. Ochi. 2002. A rifampicin resistance mutation in the rpoB gene confers ppGpp-independent antibiotic production in Streptomyces coelicolor A3(2). Mol. Genet. Genomics 268:179-189.
42. Youngman, E. M., S. L. He, L. J. Nikstad, and R. Green. 2007. Stop codon recognition by release factors induces structural rearrangement of the ribosomal decoding center that is productive for peptide release. Mol. Cell 28:533-543.
43. Zengel, J. M., R. Young, P. P. Dennis, and M. Nomura. 1977. Role of ribosomal protein S12 in peptide chain elongation: analysis of pleiotropic, streptomycin-resistant mutants of Escherichia coli. J. Bacteriol. 129:1320-1329.