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.
| Original language | American English |
|---|---|
| Article number | 113072 |
| Journal | Cell Reports |
| Volume | 42 |
| Issue number | 9 |
| DOIs | |
| State | Published - 26 Sep 2023 |
Bibliographical note
Funding Information:The authors are grateful to Dr. Michal Bronstein and Ms. Adi Turjeman (The Center for Genomic Technologies of the Alexander Silberman Institute of Life Sciences, The Hebrew University) for their help with high-throughput sequencing. The authors would like to thank Dr. Uri Gat and Prof. Yehuda Tzfati (The Hebrew University) for granting access and guidance using their lab equipment. In addition, the authors would like to thank Dr. Grigory Genikhovich (University of Vienna) for material and protocol exchange during the early stages this project’s establishment. A.F. was supported by EMBO Short Term Fellowship 8417 and Long Term Fellowship 914-2021 during parts of this work. This work was funded by the European Research Council Starting Grant (CNIDARIAMICRORNA, 637456 ) and Consolidator Grant (AntiViralEvo, 863809 ) to Y.M.
Funding Information:
The authors are grateful to Dr. Michal Bronstein and Ms. Adi Turjeman (The Center for Genomic Technologies of the Alexander Silberman Institute of Life Sciences, The Hebrew University) for their help with high-throughput sequencing. The authors would like to thank Dr. Uri Gat and Prof. Yehuda Tzfati (The Hebrew University) for granting access and guidance using their lab equipment. In addition, the authors would like to thank Dr. Grigory Genikhovich (University of Vienna) for material and protocol exchange during the early stages this project's establishment. A.F. was supported by EMBO Short Term Fellowship 8417 and Long Term Fellowship 914-2021 during parts of this work. This work was funded by the European Research Council Starting Grant (CNIDARIAMICRORNA, 637456) and Consolidator Grant (AntiViralEvo, 863809) to Y.M. Y.M. and A.F. conceptualized the study and designed the experiments. A.F. carried out the experiments in Nematostella assisted by J.M.S. (RNA library preparation), I.K. (FACS), and A.M.T. (qPCR). In Hydractinia, experimental design was carried out by U.F. and M.S.-S. who performed the experiments. E.C. contributed to experimental optimization. RNA sequencing data and single-cell expression data analysis was carried out by J.M.S. Y.M. and A.F. wrote the paper. All authors commented on and edited the text. The authors declare no competing interests.
Publisher Copyright:
© 2023 The Authors
Keywords
- CP: Developmental biology
- CP: Molecular biology
- Cnidaria
- Hydractinia
- cnidocyte
- microRNA
- nematocyte Nematostella
- post-transcriptional regulation