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

doi:10.1016/j.celrep.2023.113072

An ancient pan-cnidarian microRNA regulates stinging capsule biogenesis in Nematostella vectensis

Cell Rep. 2023 Sep 26;42(9):113072. doi: 10.1016/j.celrep.2023.113072. Epub 2023 Sep 6.

Authors

Arie Fridrich¹, Miguel Salinas-Saaverda², Itamar Kozlolvski³, Joachim M Surm³, Eleni Chrysostomou², Abhinandan M Tripathi³, Uri Frank², Yehu Moran⁴

Affiliations

¹ 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. Electronic address: arie.fridrich@gmi.oeaw.ac.at.
² Centre for Chromosome Biology, University of Galway, Galway, Ireland.
³ Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.
⁴ Department of Ecology Evolution and Behavior, Faculty of Science, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel. Electronic address: yehu.moran@mail.huji.ac.il.

Abstract

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.

Keywords: CP: Developmental biology; CP: Molecular biology; Cnidaria; Hydractinia; cnidocyte; microRNA; nematocyte Nematostella; post-transcriptional regulation.