Heterogeneous rRNAs are differentially expressed during the morphological development of Streptomyces coelicolor

It is generally assumed that all mature rRNA molecules assembled into ribosomes within a single cell are identical. However, sequence analysis of Streptomyces coelicolor genome revealed that it harbors six copies of divergent rRNA operons that may express and constitute three and five different kinds of small subunit (SSU) and large subunit (LSU) rRNA molecules, respectively, in a single cell. Phylogenetic analyses of the LSU rRNA genes and the internal transcribed spacer between SSU and LSU genes indicated that the LSU gene of rrnA and rrnE operons might be the result of interspecies recombination between rRNA genes in closely related streptomycetes. Profiling of rRNA species using primer extension analysis showed that heterogeneous rRNA transcripts are expressed and assembled into ribosomes in the cell. As the cells developed from germination to sporulation, the relative amount of LSU rRNA molecules derived from three rRNA operons (rrnA, D, and E) gradually decreased from similar to 85% to similar to 60%, whereas the distribution of LSU rRNA molecules from two other operons (rrnB and F) and rrnC operon gradually increased from similar to 10% to similar to 20% of the total LSU rRNA. These findings indicate that heterogeneous rRNA molecules are differentially expressed during the life cycle of this developmentally complex microorganism.