Unicellular origin of the animal microRNA machinery

Bråte, J., Neumann, S. R., Fromm, B., Haraldsen, A. A. B., Tarver, J. E., Suga, H., Donoghue, P. C. J., Peterson, K. J., Ruiz-Trillo, I, Grini, P. E. and Shalchian-Tabrizi, K. 2018. Current Biology. doi:10.1016/j.cub.2018.08.018

Here we show for the first time that unicellular ancestors of animals have both microRNAs and the microRNA biogenesis machinery found in animals. This means that the origin of the animal miRNA machinery was independent of animal multicellularity.

Distribution of miRNA machinery components Domain composition of Ichthyosporean miRNA macinery genes Phylogenetic analysis of Drosha and Pasha Expression of ichthyosporean pre-miRNA

Abstract

The emergence of multicellular animals was associated with an increase in phenotypic complexity and with the acquisition of spatial cell differentiation and embryonic development. Paradoxically, this phenotypic transition was not paralleled by major changes in the underlying developmental toolkit and regulatory networks. In fact, most of these systems are ancient, established already in the unicellular ancestors of animals. In contrast, the Microprocessor protein machinery, which is essential for microRNA (miRNA) biogenesis in animals, as well as the miRNA genes themselves produced by this Microprocessor, have not been idenpngied outside of the animal kingdom. Hence, the Microprocessor, with the key proteins Pasha and Drosha, is regarded as an animal innovation. Here, we challenge this evolutionary scenario by investigating unicellular sister lineages of animals through genomic and transcriptomic analyses. We idenpngy in Ichthyosporea both Drosha and Pasha (DGCR8 in vertebrates), indicating that the Microprocessor complex evolved long before the last common ancestor of animals, consistent with a pre-metazoan origin of most of the animal developmental gene elements. Through small RNA sequencing, we also discovered expressed bona fide miRNA genes in several species of the ichthyosporeans harboring the Microprocessor. A deep, pre-metazoan origin of the Microprocessor and miRNAs comply with a view that the origin of multicellular animals was not directly linked to the innovation of these key regulatory components.