Diversification of a single ancestral gene into a successful toxin superfamily in highly venomous Australian funnel-web spiders

Pineda, Sandy S., Sollod, Brianna L., Wilson, David, Darling, Aaron, Sunagar, Kartik, Undheim, Eivind A.B., Kely, Laurence, Antunes, Agostino, Fry, Bryan G., and King, Glenn F. (2014) Diversification of a single ancestral gene into a successful toxin superfamily in highly venomous Australian funnel-web spiders. BMC Genomics, 15. 177. pp. 1-16.

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Abstract

Background: Spiders have evolved pharmacologically complex venoms that serve to rapidly subdue prey and deter predators. The major toxic factors in most spider venoms are small, disulfide-rich peptides. While there is abundant evidence that snake venoms evolved by recruitment of genes encoding normal body proteins followed by extensive gene duplication accompanied by explosive structural and functional diversification, the evolutionary trajectory of spider-venom peptides is less clear.

Results: Here we present evidence of a spider-toxin superfamily encoding a high degree of sequence and functional diversity that has evolved via accelerated duplication and diversification of a single ancestral gene. The peptides within this toxin superfamily are translated as prepropeptides that are posttranslationally processed to yield the mature toxin. The N-terminal signal sequence, as well as the protease recognition site at the junction of the propeptide and mature toxin are conserved, whereas the remainder of the propeptide and mature toxin sequences are variable. All toxin transcripts within this superfamily exhibit a striking cysteine codon bias. We show that different pharmacological classes of toxins within this peptide superfamily evolved under different evolutionary selection pressures.

Conclusions: Overall, this study reinforces the hypothesis that spiders use a combinatorial peptide library strategy to evolve a complex cocktail of peptide toxins that target neuronal receptors and ion channels in prey and predators. We show that the ω-hexatoxins that target insect voltage-gated calcium channels evolved under the influence of positive Darwinian selection in an episodic fashion, whereas the κ-hexatoxins that target insect calcium-activated potassium channels appear to be under negative selection. A majority of the diversifying sites in the ω-hexatoxins are concentrated on the molecular surface of the toxins, thereby facilitating neofunctionalisation leading to new toxin pharmacology.

Item ID: 38771
Item Type: Article (Research - C1)
ISSN: 1471-2164
Keywords: Spider toxin; Spider venom; Hexatoxin; ω-hexatoxin; κ-hexatoxin; Australian funnel-web spider; molecular evolution; gene duplication; positive selection; negative selection
Additional Information:

© 2014 Pineda et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Funders: Australian Research Council (ARC), National Science Foundation (USA), University of Queensland (UQ), Fundação para a Ciência e a Tecnologia, Portugal
Projects and Grants: ARC DP0774245, ARC DP1095728, NSF MCB9983242, FCT project PTDC/AAC-AMB/121301/2010 (FCOMP-01-0124-FEDER-019490), FCT project PesT-C/MAR/LA0015/2011
Date Deposited: 20 May 2015 04:09
FoR Codes: 06 BIOLOGICAL SCIENCES > 0601 Biochemistry and Cell Biology > 060199 Biochemistry and Cell Biology not elsewhere classified @ 100%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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