A recent evolutionary origin of a bacterial small RNA that controls multicellular fruiting body development

Abstract

In animals and plants, non-coding small RNAs regulate the expression of many genes at the post-transcriptional level. Recently, many non-coding small RNAs (sRNAs) have also been found to regulate a variety of important biological processes in bacteria, including social traits, but little is known about the phylogenetic or mechanistic origins of such bacterial sRNAs. Here we propose a phylogenetic origin of the myxobacterial sRNA Pxr, which negatively regulates the initiation of fruiting body development in Myxococcus xanthus as a function of nutrient level, and also examine its diversification within the Myxococcocales order. Homologs of pxr were found throughout the Cystobacterineae suborder (with a few possible losses) but not outside this clade, suggesting a single origin of the Pxr regulatory system in the basal Cystobacterineae lineage. Rates of pxr sequence evolution varied greatly across Cystobacterineae sub-clades in a manner not predicted by overall genome divergence. A single copy of pxr was found in most species with 17% of nucleotide positions being polymorphic among them. However three tandem paralogs were present within the genus Cystobacter and these alleles together exhibited an elevated rate of divergence. There appears to have been strong selection for maintenance of a predicted stem-loop structure, as polymorphisms accumulated preferentially at loop or bulge regions or as complementary substitutions within predicted stems. All detected pxr homologs are located in the intergenic region between the σ54-dependent response regulator nla19 and a predicted NADH dehydrogenase gene, but other neighboring gene content has diversified.