Monosomes and polysomes bind functionally distinct classes of protein-coding and noncoding RNAs

Background: The regulation of cellular protein levels involves various transcriptional and translational mechanisms. On the translational level one variable is the transition from a monosomal to a polysomal configuration. We characterized the coding and noncoding RNA content of monosomes and polysomes of a human cell line by RNA sequencing. Results: We show that many transcripts are enriched in either the monosomal or the polysomal fraction, rather than showing an even distribution. Preferred ribosomal occupation of protein-coding transcripts was found to depend on the length of the mRNA and on the biological function of the encoded protein. Interestingly, we also find many long noncoding RNAs associated with ribosomes. 425 long noncoding RNAs are specifically enriched in the ribosomal fractions, compared to only 79 in the nuclear fraction. The ribosome-associated long non-coding RNAs show a preference for binding either mono- or polyribosomes and this is independent of transcript length. Conclusions: Monosomes and polysomes bind distinct sets of mRNA molecules and the preferred ribosomal configuration depends on the cellular function of the encoded protein. The requirements for protein level dynamics are different for divergent cellular processes, and these differences in dynamics may thus in part be established at the monosomal to polysomal transition. Interestingly, we demonstrate that many lncRNAs are enriched at ribosomal sites, suggesting a potential functional role of these noncoding transcripts in regulation of the translation machinery.