Abstract
Most bacterial small RNAs (sRNAs) are post-transcriptional regulators of gene expression, exerting their regulatory function by base-pairing with their target mRNAs. While it has become evident that sRNAs play central regulatory roles in the cell, little is known about their evolution and the evolution of their regulatory interactions. Here we used the prokaryotic phylogenetic tree to reconstruct the evolutionary history of Escherichia coli sRNAs and their binding sites on target mRNAs. We discovered that sRNAs currently present in E. coli mainly accumulated inside the Enterobacteriales order, succeeding the appearance of other types of noncoding RNAs and concurrently with the evolution of a variant of the Hfq protein exhibiting a longer C-terminal region. Our analysis of the evolutionary ages of sRNA-mRNA interactions revealed that while all sRNAs were evolutionarily older than most of their known binding sites on mRNA targets, for quite a few sRNAs there was at least one binding site that coappeared with or preceded them. It is conceivable that the establishment of these first interactions forced selective pressure on the sRNAs, after which additional targets were acquired by fitting a binding site to the active region of the sRNA. This conjecture is supported by the appearance of many binding sites on target mRNAs only after the sRNA gain, despite the prior presence of the target gene in ancestral genomes. Our results suggest a selective mechanism that maintained the sRNAs across the phylogenetic tree, and shed light on the evolution of E. coli post-transcriptional regulatory network.
Highlights
It is well established that many transcribed genes are not further translated to proteins but rather function in the cell as noncoding RNAs
Our analysis revealed that the “other noncoding RNAs (ncRNAs)” appeared first, along with several cis-acting ncRNA families that continued to accumulate later on, while the E. coli trans-acting small RNAs (sRNAs) were the latest to appear in evolution (P < 7 × 10−5 in two-tailed Mann-Whitney test comparing the evolutionary ages of cis- and trans-acting ncRNAs) (Fig. 1; Supplemental Table S1)
Since the function of most sRNAs relies on their base-pairing with their targets, it was suggested that establishment of a regulatory interaction between a sRNA and a mRNA should impose a selective pressure to maintain the sRNA (Gottesman and Storz 2011; Richter and Backofen 2012)
Summary
It is well established that many transcribed genes are not further translated to proteins but rather function in the cell as noncoding RNAs (ncRNAs). Small regulatory RNAs involved in the post-transcriptional regulation of gene expression were discovered in all kingdoms of life and were shown to play important roles in the regulation of central cellular processes (for reviews, see Bartel 2009; Carthew and Sontheimer 2009; Waters and Storz 2009). NcRNAs are utilized in various ways to regulate mRNA and protein levels of many genes. Regulatory ncRNAs can be classified into two types. The first type involves RNA elements that are transcribed as part of their target gene (usually at the 5′ end) to regulate its transcrip-
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