Heterogeneous rRNA Molecules Encoded by Streptomyces coelicolor M145 Genome are All Expressed and Assembled into Ribosomes

  • Kim, Hyun-Lee (Graduate School of Life Science and Biotechnology, Pochon CHA University) ;
  • Shin, Eun-Kyoung (Department of Life Science, Chung-Ang University) ;
  • Kim, Hong-Man (Department of Life Science, Chung-Ang University) ;
  • Go, Ha-Young (Department of Life Science, Chung-Ang University) ;
  • Roh, Jae-Sook (Department of Pharmacological Research, National Institute of Toxicological Research) ;
  • Bae, Jee-Hyeon (Graduate School of Life Science and Biotechnology, Pochon CHA University) ;
  • Lee, Kang-Seok (Department of Life Science, Chung-Ang University)
  • Published : 2007.10.30

Abstract

The Streptomyces coelicolor M145 genome harbors six copies of divergent rRNA operons that differ at ${\sim}0.2%$ and ${\sim}0.6%$ of the nucleotide positions in small subunit (SSU) and large subunit (LSD) rRNA genes, respectively. When these rRNA genes are expressed, a single cell may harbor three different kinds of SSU rRNA and five kinds of LSU rRNA. Primer extension analyses revealed that all of the heterogeneous rRNA molecules are expressed and assembled into ribosomes. This finding and the maintenance of the intragenomic variability of rRNA operons imply the existence of functional divergence of rRNA species in this developmentally complex microorgamsm.

Keywords

References

  1. Baylis, H. A. and M. J. Bibb. 1988. Organisation of the ribosomal RNA genes in Streptomyces coelicolor A3(2). Mol. Gen. Genet. 211: 191-196 https://doi.org/10.1007/BF00330593
  2. Bouncher, Y., C. J. Douady, A. K. Sharma, M. Kamekura, and W. F. Doolittle. 2004. Intragenomic heterogeneity and intergenomic recombination among Haloarchaeal rRNA genes. J. Bacteriol. 186: 3980-3990 https://doi.org/10.1128/JB.186.12.3980-3990.2004
  3. Cannone, J. J., S. Subramanian, M. N. Schnare, J. R. Collett, L. M. D'Souza, Y. Du, B. Feng, N. Lin, L. V. Madabusi, K. M. Muller, N. Pande, Z. Shang, N. Yu, and R. R. Gutell. 2002. The comparative RNA Web (CRW) site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3: 2 https://doi.org/10.1186/1471-2105-3-32
  4. Farina, M., S. Stira, R. Mancuso, and C. Grisanti. 1996. Characterization of Streptomyces venezuelae ATCC 10595 rRNA gene clusters and cloning of rrnA. J. Bacteriol. 178: 1480-1483 https://doi.org/10.1128/jb.178.5.1480-1483.1996
  5. Gunderson, J. H., M. L. Sogin, G. Wollett, M. Hollingdale, V. F. Cruz, A. P. Waters, and T. F. McCutchan. 1987. Structurally distinct, stage specific ribosomes occur in Plasmodium. Science 238: 933-937 https://doi.org/10.1126/science.3672135
  6. Ikeda, H., J. Ishikawa, A. Hanamato, M. Shinose, H. Kikuchi, T. Shiba, Y. Sakaki, M. Hattori, and S. Omura. 2003. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21: 526-531 https://doi.org/10.1038/nbt820
  7. Kim, E., H. Kim, S. Hong, K. H. Kang, Y. E. Kho, and Y. Park. 1993. Gene organization and primary structure of a ribosomal RNA gene cluster from Streptomyces griseus subsp. griseus. Gene 132: 21-31 https://doi.org/10.1016/0378-1119(93)90510-A
  8. Lee, K., S. Varma, J. Santalucia Jr., and P. R. Cunningham. 1997. In vivo determination of RNA structure-function relationships: Analysis of the 790 loop in ribosomal RNA. J. Mol. Biol. 269: 732-743 https://doi.org/10.1006/jmbi.1997.1092
  9. Pernodet, J. L., F. Boccard, M. T. Alegre, J. Gangat, and M. Guerineau. 1983. Organization and nucleotide sequence analysis of a ribosomal RNA gene cluster from Streptomyces ambofaciens. Gene 79: 33-46
  10. Plohl, M. and V. Gamulin. 1991. Sequence of the 5S rRNA gene and organization of ribosomal RNA operons in Streptomyces rimosus. FEMS Microbiol. Lett. 77: 139-143 https://doi.org/10.1111/j.1574-6968.1991.tb04337.x
  11. Powers, T. and H. F. Noller. 1991. A functional pseudoknot in 16S ribosomal RNA. EMBO J. 10: 2203-2214
  12. Ryou, S. M., J. M. Kim, J. H. Yeom, H. L. Kim, H. Y. Go, E. K. Shin, and K. Lee. 2005. Species-specific cleavage by RNase E-like enzymes in 5S rRNA maturation. J. Microbiol. Biotechnol. 15: 1100-1105
  13. Ryu, Y. G., E. S. Kim, D. W. Kim, S. K. Kim, and K. J. Lee. 2007. Differential stringent responses of Streptomyces coelicolor M600 to starvation of specific nutrients. J. Microbiol. Biotechnol. 17: 305-312
  14. Shuang, J. L., C. H. Lui, S. Q. An, Y. Xing, G. Q. Zheng, and Y. F. Shen. 2006. Some universal characteristics of intertidal bacterial diversity as revealed by 16S rRNA gene-based PCR clone analysis. J. Microbiol. Biotechnol. 16: 1882-1889
  15. Suzuki, Y., Y. Ono, A. Nagata, and T. Yamada. 1988. Molecular cloning and characterization of an rRNA operon in Streptomyces lividans TK21. J. Bacteriol. 170: 1631-1636 https://doi.org/10.1128/jb.170.4.1631-1636.1988
  16. Szatkiewicz, J. P., H. Cho, S. M. Ryou, J. M. Kim, P. R. Cunningham, and K. Lee. 2006. Genetic analysis of a structural motif within the conserved 530 stem-loop of Escherichia coli 16S rRNA. J. Microbiol. Biotechnol. 16: 569-575
  17. Yap, W. H. and Y. Wang. 1999. Molecular cloning and comparative sequence analyses of rRNA operons in Streptomyces nodosus ATCC 14899. Gene 232: 77-85 https://doi.org/10.1016/S0378-1119(99)00112-2
  18. Zhao, X.-Q., K.-R. Kim, L.-W. Sang, S.-H. Kang, Y.-Y. Yang, and J.-W. Suh. 2005. Genetic organization of a 50-kb gene cluster isolated from Streptomyces kanamyceticus for kanamycin biosynthesis and characterization of kanamycin acetyltransferase. J. Microbiol. Biotechnol. 15: 346-353