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Open Access Highly Accessed Research article

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

Sandy S Pineda1, Brianna L Sollod27, David Wilson138, Aaron Darling19, Kartik Sunagar45, Eivind A B Undheim16, Laurence Kely6, Agostinho Antunes45, Bryan G Fry16* and Glenn F King1*

Author Affiliations

1 Institute for Molecular Bioscience, The University of Queensland, 306 Carmody Road, St Lucia, QLD 4072, Australia

2 Department of Molecular, Microbial & Structural Biology, School of Medicine, University of Connecticut, Farmington, CT 06030, USA

3 Xenome, P.O. Box 1024, Indooroopilly Centre, QLD 4068, Australia

4 CIMAR/CIIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Universidade do Porto, Rua dos Bragas, 177, 4050-123 Porto, Portugal

5 Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal

6 Venom Evolution Lab, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia

7 Current address: Monsanto Company, 800 N. Lindbergh Blvd, St. Louis, MO 63167, USA

8 Current address: Faculty of Medicine, Health and Molecular Science-Queensland, Tropical Health Alliance, James Cook University, Cairns, Queensland, Australia

9 Current address: The i3 Institute, University of Technology Sydney, Ultimo, NSW 2007, Australia

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BMC Genomics 2014, 15:177  doi:10.1186/1471-2164-15-177

Published: 5 March 2014

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.

Keywords:
Spider toxin; Spider venom; Hexatoxin; ω-hexatoxin; κ-hexatoxin; Australian funnel-web spider; Molecular evolution; Gene duplication; Positive selection; Negative selection