Evolution of an ancient venom: recognition of a novel family of cnidarian toxins and the common evolutionary origin of sodium and potassium neurotoxins in sea anemone

Jouiaei, Mahdokht, Sunagar, Kartik, Gross, Aya Federman, Scheib, Holger, Alewood, Paul F., Moran, Yehu and Fry, Bryan (2015) Evolution of an ancient venom: recognition of a novel family of cnidarian toxins and the common evolutionary origin of sodium and potassium neurotoxins in sea anemone. Molecular Biology and Evolution, 32 6: 1598-1610. doi:10.1093/molbev/msv050


Author Jouiaei, Mahdokht
Sunagar, Kartik
Gross, Aya Federman
Scheib, Holger
Alewood, Paul F.
Moran, Yehu
Fry, Bryan
Title Evolution of an ancient venom: recognition of a novel family of cnidarian toxins and the common evolutionary origin of sodium and potassium neurotoxins in sea anemone
Journal name Molecular Biology and Evolution   Check publisher's open access policy
ISSN 0737-4038
1537-1719
Publication date 2015-06-06
Year available 2015
Sub-type Article (original research)
DOI 10.1093/molbev/msv050
Open Access Status DOI
Volume 32
Issue 6
Start page 1598
End page 1610
Total pages 13
Place of publication Cary, NC United States
Publisher Oxford University Press
Collection year 2016
Language eng
Formatted abstract
Despite Cnidaria (sea anemones, corals, jellyfish, and hydroids) being the oldest venomous animal lineage, structure–function relationships, phyletic distributions, and the molecular evolutionary regimes of toxins encoded by these intriguing animals are poorly understood. Hence, we have comprehensively elucidated the phylogenetic and molecular evolutionary histories of pharmacologically characterized cnidarian toxin families, including peptide neurotoxins (voltage-gated Na+ and K+ channel-targeting toxins: NaTxs and KTxs, respectively), pore-forming toxins (actinoporins, aerolysin-related toxins, and jellyfish toxins), and the newly discovered small cysteine-rich peptides (SCRiPs). We show that despite long evolutionary histories, most cnidarian toxins remain conserved under the strong influence of negative selection—a finding that is in striking contrast to the rapid evolution of toxin families in evolutionarily younger lineages, such as cone snails and advanced snakes. In contrast to the previous suggestions that implicated SCRiPs in the biomineralization process in corals, we demonstrate that they are potent neurotoxins that are likely involved in the envenoming function, and thus represent the first family of neurotoxins from corals. We also demonstrate the common evolutionary origin of type III KTxs and NaTxs in sea anemones. We show that type III KTxs have evolved from NaTxs under the regime of positive selection, and likely represent a unique evolutionary innovation of the Actinioidea lineage. We report a correlation between the accumulation of episodically adaptive sites and the emergence of novel pharmacological activities in this rapidly evolving neurotoxic clade.
Keyword Cnidaria
Sodium channel toxins
Potassium channel toxins
Phylogeny
Disulfide-rich toxins
Positive selection
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2016 Collection
School of Biological Sciences Publications
Institute for Molecular Bioscience - Publications
 
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Created: Mon, 13 Apr 2015, 15:47:54 EST by Susan Allen on behalf of Institute for Molecular Bioscience