An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis
Arie Fridrich,
Miguel Salinas-Saaverda,
Itamar Kozlolvski,
Joachim M. Surm,
Eleni Chrysostomou,
Abhinandan M. Tripathi,
Uri Frank,
Yehu Moran
Affiliations
Arie Fridrich
Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel; Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, Vienna, Austria; Corresponding author
Miguel Salinas-Saaverda
Centre for Chromosome Biology, University of Galway, Galway, Ireland
Itamar Kozlolvski
Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
Joachim M. Surm
Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
Eleni Chrysostomou
Centre for Chromosome Biology, University of Galway, Galway, Ireland
Abhinandan M. Tripathi
Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel
Uri Frank
Centre for Chromosome Biology, University of Galway, Galway, Ireland
Yehu Moran
Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel; Corresponding author
Summary: An ancient evolutionary innovation of a novel cell type, the stinging cell (cnidocyte), appeared >600 million years ago in the phylum Cnidaria (sea anemones, corals, hydroids, and jellyfish). A complex bursting nano-injector of venom, the cnidocyst, is embedded in cnidocytes and enables cnidarians to paralyze their prey and predators, contributing to this phylum’s evolutionary success. In this work, we show that post-transcriptional regulation by a pan-cnidarian microRNA, miR-2022, is essential for biogenesis of these cells in the sea anemone Nematostella vectensis. By manipulation of miR-2022 levels in a transgenic reporter line of cnidocytes, followed by transcriptomics, single-cell data analysis, prey paralysis assays, and cell sorting of transgenic cnidocytes, we reveal that miR-2022 enables cnidocyte biogenesis in Nematostella, while exhibiting a conserved expression domain with its targets in cnidocytes of other cnidarian species. Thus, here we revealed a functional basis to the conservation of one of nature’s most ancient microRNAs.
