Early origins and evolution of microRNAs and Piwi-interacting RNAs in animals

In bilaterian animals, such as humans, flies and worms, hundreds of microRNAs (miRNAs), some conserved throughout bilaterian evolution, collectively regulate a substantial fraction of the transcriptome. In addition to miRNAs, other bilaterian small RNAs, known as Piwi-interacting RNAs (piRNAs), protect the genome from transposons. Here we identify small RNAs from animal phyla that diverged before the emergence of the Bilateria. The cnidarian Nematostella vectensis (starlet sea anemone), a close relative to the Bilateria, possesses an extensive repertoire of miRNA genes, two classes of piRNAs and a complement of proteins specific to small-RNA biology comparable to that of humans. The poriferan Amphimedon queenslandica (sponge), one of the simplest animals and a distant relative of the Bilateria, also possesses miRNAs, both classes of piRNAs and a full complement of the small-RNA machinery. Animal miRNA evolution seems to have been relatively dynamic, with precursor sizes and mature miRNA sequences differing greatly between poriferans, cnidarians and bilaterians. Nonetheless, miRNAs and piRNAs have been available as classes of riboregulators to shape gene expression throughout the evolution and radiation of animal phyla. MicroRNAs an early feature of metazoans MicroRNAs, the small inhibitory RNA molecules discovered in 1993 in the roundworm Caenorhabditis elegans , are widely distributed in complex animals. It is commonly assumed that they arose as a way to fine-tune gene expression when animals developed bilateral symmetry — becoming complicated enough to have anterior and posterior ends as well as a top and bottom. But new work, based on sequencing the total RNA content of representatives of three basal metazoan phyla (a placozoan, a sponge and a sea anemone) and a unicellular choanoflagellate suggests that microRNA has been around for much longer than was thought. It seems that the regulatory microRNA pathway arose very early in metazoan evolution — when multicellularity emerged — although the machinery was subsequently lost in some lineages.