Browse > Article

Genetic Characterization of Two S-Adenosylmethionine-induced ABC Transporters Reveals Their Roles in Modulations of Secondary Metabolism and Sporulation in Streptomyces coelicolor M145  

Shin, Su-Kyoung (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University)
Park, Hyun-Suh (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University)
Kwon, Hyung-Jin (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University)
Yoon, Hyun-Jin (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University)
Suh, Joo-Won (Department of Biological Science, Institute of Bioscience and Biotechnology, Myongji University)
Publication Information
Journal of Microbiology and Biotechnology / v.17, no.11, 2007 , pp. 1818-1825 More about this Journal
Abstract
S-Adenosylmethionine (SAM) was previously documented to activate secondary metabolism in a variety of Streptomyces spp. and to promote actinorhodin (ACT) and undecylprodigiosin (RED) in Streptomyces coelicolor. The SAM-induced proteins in S. coelicolor include several ABC transporter components (SCO5260 and SCO5477) including BldKB, the component of a well-known regulatory factor for differentiations. In order to assess the role of these ABC transporter complexes in differentiation of Streptomyces, SCO5260 and SCO5476, the first genes from the cognate complex clusters, were individually inactivated by gene replacement. Inactivation of either SCO5260 or SCO5476 led to impaired sporulation on agar medium, with the more drastic defect in the SCO5260 null mutant (${\Delta}SCO5260$). ${\Delta}SCO5260$ displayed growth retardation and reduced yields of ACT and RED in liquid cultures. In addition, SAM supplementation failed in promoting the production of ACT and RED in ${\Delta}SCO5260$. Inactivation of SCO5476 gave no significant change in growth and production of ACT and RED, but impaired the promoting effect of SAM on ACT production without interfering with the effect on RED production. The present study suggests that SAM induces several ABC transporters to modulate secondary metabolism and morphological development in S. coelicolor.
Keywords
S-Adenosylmethionine; ABC transporter; gene inactivation; secondary metabolism; sporulation; Streptomyces coelicolor;
Citations & Related Records
Times Cited By KSCI : 4  (Citation Analysis)
Times Cited By Web Of Science : 7  (Related Records In Web of Science)
연도 인용수 순위
1 Bentley, S. D., K. F. Chater, A. M. Cerdeno-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147   DOI   ScienceOn
2 Chong, Y., J. Young, J. Kim, Y. Lee, K. S. Park, J. H. Cho, H. J. Kwon, J. W. Suh, and Y. Lim. 2006. S-Adenosyl-L-methionine analogues to enhance the production of actinorhodin. J. Microbiol. Biotechnol. 16: 1154-1157   과학기술학회마을
3 Detmers, F. J., F. C. Lanfermeijer, and B. Poolman. 2001. Peptides and ATP binding cassette peptide transporters. Res. Microbiol. 152: 245-258   DOI   ScienceOn
4 Hodgson, D. A. 2000. Primary metabolism and its control in streptomycetes: A most unusual group of bacteria. Adv. Microb. Physiol. 42: 47-238   DOI
5 Kim, D. W., K. F. Chater, K. J. Lee, and A. Hesketh. 2005. Effects of growth phase and the developmentally significant bldA-specific tRNA on the membrane-associated proteome of Streptomyces coelicolor. Microbiology 151: 2707-2720   DOI   ScienceOn
6 Ma, H. and K. Kendall. 1994. Cloning and analysis of a gene cluster from Streptomyces coelicolor that causes accelerated aerial mycelium formation in Streptomyces lividans. J. Bacteriol. 176: 3800-3811   DOI
7 Magnuson, R., J. Solomon, and A. D. Grossman. 1994. Biochemical and genetic characterization of a competence pheromone from B. subtilis. Cell 77: 207-216   DOI   ScienceOn
8 Susstrunk, U., J. Pidoux, S. Taubert, A. Ullmann, and C. J. Thompson. 1998. Pleiotropic effects of cAMP on germination, antibiotic biosynthesis, and morphological development in Streptomyces coelicolor. Mol. Microbiol. 30: 33-46   DOI   ScienceOn
9 Ueda, K., H. Takano, M. Nishimoto, H. Inaba, and T. Beppu. 2005. Dual transcriptional control of amfTSBA, which regulates the onset of cellular differentiation in Streptomyces griseus. J. Bacteriol. 187: 135-142   DOI   ScienceOn
10 Yang, Y. Y., X. Q. Zhao, Y. Y. Jin, J. H. Huh, J. H. Cheng, D. Singh, H. J. Kwon, and J. W. Suh. 2006. Novel function of cytokinin: A signaling molecule for promotion of antibiotic production in streptomycetes. J. Microbiol. Biotechnol. 16: 896-900   과학기술학회마을
11 Havarstein, L. S., G. Coomaraswamy, and D. A. Morrison. 1995. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92: 11140-11144
12 Nguyen, K. T., J. M. Willey, L. D. Nguyen, L. T. Nguyen, P. H. Viollier, and C. J. Thompson. 2002. A central regulator of morphological differentiation in the multicellular bacterium Streptomyces coelicolor. Mol. Microbiol. 46: 1223-1238   DOI   ScienceOn
13 Nodwell, J. R., K. McGovern, and R. Losick. 1996. An oligopeptide permease responsible for the import of an extracellular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol. Microbiol. 22: 881-893   DOI   ScienceOn
14 Chater, K. F. and G. Chandra. 2006. The evolution of development in Streptomyces analysed by genome comparisons. FEMS Microbiol. Rev. 30: 651-672   DOI   ScienceOn
15 Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces Genetics. The John Innes Foundation, Norwich, England
16 Zhao, X. Q., Y. Y. Jin, H. J. Kwon, Y. Y. Yang, and J. W. Suh. 2006. S-Adenosylmethionine (SAM) regulates antibiotic biosynthesis in Streptomyces spp. in a mode independent of its role as a methyl donor. J. Microbiol. Biotechnol. 16: 927-932   과학기술학회마을
17 Leonard, B. A. B., A. Podbielski, P. J. Hedberg, and G. M. Dunny. 1996. Enterococcus faecalis pheromone binding protein, PrgZ, recruits a chromosomal oligopeptide permease system to import sex pheromone cCF10 for induction of conjugation. Proc. Natl. Acad. Sci. USA 93: 260-264
18 Willey, J. M., A. Willems, S. Kodani, and J. R. Nodwell. 2006. Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol. Microbiol. 59: 731-742   DOI   ScienceOn
19 Gust, B., G. L. Challis, K. Fowler, T. Kieser, and K. F. Chater. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. USA 100: 1541-1546
20 Sanchez-Aguayo, I., J. M. Rodriguez-Galán, R. García, J. Torreblanca, and J. M. Pardo. 2004. Salt stress enhances xylem development and expression of S-adenosyl-L-methionine synthetase in lignifying tissues of tomato plants. Planta 220: 278-285   DOI   ScienceOn
21 Nodwell, J. R., M. Yang, D. Kuo, and R. Losick. 1999. Extracellular complementation and the identification of additional genes involved in aerial mycelium formation in Streptomyces coelicolor. Genetics 151: 569-584
22 Linton, K. J. and C. F. Higgins. 1998. The Escherichia coli ATP-binding cassette (ABC) proteins. Mol. Microbiol. 28: 5-13   DOI   ScienceOn
23 Dunny, G. M. and B. A. Leonard. 1997. Cell-cell communication in Gram-positive bacteria. Annu. Rev. Microbiol. 51: 557-564
24 Levdikov, V. M., E. V. Blagova, J. A. Brannigan, L. Wright, A. A. Vagin, and A. J. Wilkinson. 2005. The structure of the oligopeptide-binding protein, AppA, from Bacillus subtilis in complex with a nonapeptide. J. Mol. Biol. 345: 879-892   DOI   ScienceOn
25 Novotna, J., J. Vohradsky, P. Berndt, H. Gramajo, H. Langen, X. M. Li, W. Minas, L. Orsaria, D. Roeder, and C. J. Thompson. 2003. Proteomic studies of diauxic lag in the differentiating prokaryotes Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol. Microbiol. 48: 1289-1303   DOI   ScienceOn
26 Abouhamad, W. N., M. Manson, M. M. Gibson, and C. F. Higgins. 1991. Peptide transport and chemotaxis in Escherichia coli and Salmonella typhimurium: Characterization of the dipeptide permease (Dpp) and the dipeptide-binding protein. Mol. Microbiol. 5: 1035-1047   DOI   ScienceOn
27 Espartero, J., J. A. Pintor-Toro, and J. M. Pardo. 1994. Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress. Plant Mol. Biol. 25: 217-227   DOI
28 Kim, D. J., J. H. Huh, Y. Y. Yang, C. M. Kang, I. H. Lee, C. G. Hyun, S. K. Hong, and J. W. Suh. 2003. Accumulation of S-adenosyl-L-methionine enhances production of actinorhodin but inhibits sporulation in Streptomyces lividans TK23. J. Bacteriol. 185: 592-600   DOI
29 Lee, Y., J. Young, H. J. Kwon, J. W. Suh, J. Kim, Y. Chong, and Y. Lim. 2006. AdoMet derivatives induce the production of actinorhodin in Streptomyces coelicolor. J. Microbiol. Biotechnol. 16: 965-968   과학기술학회마을
30 Schroder, G., J. Eichel, S. Breinig, and J. Schroder. 1997. Three differentially expressed S-adenosylmethionine synthetases from Catharanthus roseus: Molecular and functional characterization. Plant Mol. Biol. 33: 211-222   DOI   ScienceOn
31 Podbielski, A., B. Pohl, M. Woischnik, C. Körner, K. H. Schmidt, E. Rozdzinski, and B. A. Leonard. 1996. Molecular characterization of group A streptococcal (GAS) oligopeptide permease (opp) and its effect on cysteine protease production. Mol. Microbiol. 21: 1087-1099   DOI   ScienceOn
32 Okamoto, S., A. Lezhava, T. Hosaka, Y. Okamoto-Hosoya, and K. Ochi. 2003. Enhanced expression of Sadenosylmethionine synthetase causes overproduction of actinorhodin in Streptomyces coelicolor A3(2). J. Bacteriol. 185: 601-609   DOI   ScienceOn
33 Rudner, D. Z., J. R. LeDeaux, K. Ireton, and A. D. Grossman. 1991. The spo0K locus of Bacillus subtilis is homologous to the oligopermease locus and is required for sporulation and competence. J. Bacteriol. 173: 1388-1398   DOI
34 Stragier, P. and R. Losick. 1996. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 3: 203-212
35 Van Breusegem, F., R. Dekeyser, J. Gielen, M. Van Montagu, and A. Caplan. 1994. Characterization of a S-adenosylmethionine synthetase gene in rice. Plant Physiol. 105: 1463-1464   DOI
36 Clewell, D. B., F. Y. An, S. E. Flannagan, M. Antiporta, and G. M. Dunny. 2000. Enterococcal sex pheromone precursors are part of signal sequences for surface lipoproteins. Mol. Microbiol. 35: 246-247   DOI   ScienceOn
37 Hillemann, D., A. Pühler, and W. Wohlleben. 1991. Gene disruption and gene replacement in Streptomyces via single stranded DNA transformation of integration vectors. Nucleic Acids Res. 19: 727-731   DOI
38 Chater, K. F. 2001. Regulation of sporulation in Streptomyces coelicolor A3(2): A checkpoint multiplex? Curr. Opin. Microbiol. 4: 667-673   DOI   ScienceOn
39 Shin, S. K., D. Xu, H. J. Kwon, and J. W. Suh. 2006. S-Adenosylmethionine activates adpA transcription and promotes streptomycin biosynthesis in Streptomyces griseus. FEMS Microbiol. Lett. 259: 53-59   DOI   ScienceOn
40 Nodwell, J. R. and R. Losick. 1998. Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor. J. Bacteriol. 180: 1334-1337
41 Holland, K. A. and I. B. Holland. 2005. Adventures with ABC-proteins: Highly conserved ATP-dependent transporters. Acta Microbiol. Immunol. Hung. 52: 309-322   DOI   ScienceOn
42 Park, H. S., S. K. Shin, Y. Y. Yang, H. J. Kwon, and J. W. Suh. 2005. Accumulation of S-adenosylmethionine induced oligopeptide transporters including BldK to regulate differentiation events in Streptomyces coelicolor M145. FEMS Microbiol. Lett. 249: 199-206   DOI   ScienceOn