Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom

Maria Y. Sachkova*, Morani Landau, Joachim M. Surm, Jason Macrander, Shir A. Singer, Adam M. Reitzel, Yehu Moran*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

21 Scopus citations

Abstract

The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model for characterizing the evolution of genes functioning in venom and nervous systems. Although venom has evolved independently numerous times in animals, the evolutionary origin of many toxins remains unknown. In this work, we pinpoint an ancestral gene giving rise to a new toxin and functionally characterize both genes in the same species. Thus, we report a case of protein recruitment from the cnidarian nervous to venom system. The ShK-like1 peptide has a ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Both peptides exhibit similarities in their functional activities: They provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics, and functional approaches to reveal one venom component, five neuropeptides with two different cysteine motifs, and an evolutionary pathway from nervous to venom system in Cnidaria.

Original languageAmerican English
Pages (from-to)27481-27492
Number of pages12
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number44
DOIs
StatePublished - 3 Nov 2020

Bibliographical note

Publisher Copyright:
© 2020 National Academy of Sciences. All rights reserved.

Keywords

  • Nematocyst
  • Neuron
  • Neuropeptide
  • Toxin recruitment
  • Venom evolution

Fingerprint

Dive into the research topics of 'Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom'. Together they form a unique fingerprint.

Cite this