Abstract
Bacterial genes are typically grouped into operons defined as clusters of adjacent genes encoding for proteins that fill related roles and are transcribed into a single polycistronic mRNA molecule. This simple organization provides an efficient mechanism to coordinate the expression of neighboring genes and is at the basis of gene regulation in bacteria. Here, we report the existence of a higher level of organization in operon structure that we named noncontiguous operon and consists in an operon containing a gene(s) that is transcribed in the opposite direction to the rest of the operon. This transcriptional architecture is exemplified by the genes menE-menC-MW1733-ytkD-MW1731 involved in menaquinone synthesis in the major human pathogen Staphylococcus aureus We show that menE-menC-ytkD-MW1731 genes are transcribed as a single transcription unit, whereas the MW1733 gene, located between menC and ytkD, is transcribed in the opposite direction. This genomic organization generates overlapping transcripts whose expression is mutually regulated by transcriptional interference and RNase III processing at the overlapping region. In light of our results, the canonical view of operon structure should be revisited by including this operon arrangement in which cotranscription and overlapping transcription are combined to coordinate functionally related gene expression.
Highlights
The term operon was first proposed by Jacob and Monod [1] as a functional genomic DNA unit containing a group of genes that are transcribed together under the control of a single promoter
We screened genome-wide the transcriptome data obtained from the clinical isolates S. aureus 15981 [21] and S. aureus MW2 to identify genes cotranscribed together despite being separated by a gene transcribed in the opposite direction
The novelty introduced by the noncontiguous operon concept is that genes within an operon can be interspersed with genes divergently transcribed and that, they do not necessarily need to be contiguous in the genome
Summary
The term operon was first proposed by Jacob and Monod [1] as a functional genomic DNA unit containing a group of genes that are transcribed together under the control of a single promoter. Through a genome-wide transcriptome profiling of the pathogen Staphylococcus aureus [21], we identified several examples of groups of genes that were apparently transcribed together despite that they were separated by gene(s) transcribed in the opposite direction This transcriptional organization is an extreme example of an excludon, since the mRNA encoded on the opposite strand of DNA to the operon would serve as a canonical mRNA that encodes for a protein while acting as an antisense RNA, base-pairing all along its length with an internal untranslated region of the polycistronic mRNA. The resulting mRNA is fully complementary to the operon transcript This genetic arrangement leads to mutual regulation of the overlapping transcripts expression and, provides an additional strategy for coordinating the expression of functionally related genes within an operon
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