Centipede venom evolution: casting light on a neglected group of venomous animals

Undheim, Eivind (2013). Centipede venom evolution: casting light on a neglected group of venomous animals PhD Thesis, Institute for Molecular Bioscience, The University of Queensland.

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Author Undheim, Eivind
Thesis Title Centipede venom evolution: casting light on a neglected group of venomous animals
School, Centre or Institute Institute for Molecular Bioscience
Institution The University of Queensland
Publication date 2013
Thesis type PhD Thesis
Supervisor Glenn F. King
Bryan G. Fry
Total pages 219
Total colour pages 27
Total black and white pages 192
Language eng
Subjects 0603 Evolutionary Biology
0304 Medicinal and Biomolecular Chemistry
1115 Pharmacology and Pharmaceutical Sciences
Formatted abstract
A major limitation of venom research has been the narrow taxonomical range studied, with entire groups of venomous animals remaining virtually completely unstudied. One such group is centipedes, class Chilopoda, which emerged about 420 million years ago (mya) and represents one of the oldest extant venom systems. Five centipede species were selected to provide both wide taxonomic coverage and a phylogenetic timeline to date evolutionary events. Emphasising the Scolopendridae due to their large size, availability, and clinical importance, the following species were selected to represent over 400 million years of evolution and to allow for comparisons at the order, subfamily, genus, and species level: Thereuopoda longicornis (Scutigeromorpha), Ethmostigmus rubripes (Scolopendromorpha; Scolopendridae; Otostigminae), Cormocephalus westwoodi (Scolopendridae; Scolopendrinae), Scolopendra alternans (Scolopendrinae), and Scolopendra morsitans.

Taking the complementary approaches of transcriptomics, proteomics, phylogenetics, histology, mass spectrometry imaging, scanning electron microscopy, energy dispersion spectroscopy, nuclear magnetic resonance spectroscopy and magnetic resonance imaging this thesis provides the first comprehensive insight into the chilopod venom system. Centipede venoms differ substantially from the venoms of other arthropods described to date in the prevalence of high molecular weight components as well as the presence of transcripts encoding multiple mature venom peptides (“multifunctional transcripts”). The ancient evolutionary history of centipedes is also apparent from the differences between the scolopendromorph and scutigeromorph venoms, which diverged over 400 million years ago, and appear to employ substantially different venom strategies. Despite having a venom apparatus unfit for physical overpowering of prey, scutigeromorphs appear to have a much lower peptidic and proteomic venom diversity than scolopendromorphs, perhaps relying more on non-peptidic enzymatic products. This is likely due to lack of venom gland complexity, with scolopendromorphs having 10-100 fold more “secretory units” present in each venom gland and displaying a peptidic diversity more consistent with other predatory arthropods.

Scolopendrid venoms show a high diversity in cysteine rich components that span several structural families, most of which have completely novel primary structures. One of these families, scoloptoxin family 3, is particularly exciting from a biodiscovery point of view, and two peptides with high therapeutic potential are described in collaboration with members of Prof Lai’s group at the Chinese Academy of Sciences, Kunming, China. Both peptides, one KV1.3 inhibitor (κ-SLPTX-Ssm1a) and one NaV1.7 inhibitor (μ-SLPTX-Ssm6a), assume almost completely helical secondary structures, are highly selective, and show astonishing stability. Understanding the evolutionary processes behind these ancient venom systems contributes to our understanding of which traits make peptides stable and amenable to neofunctionalisation, and may aid in directing future biodiscovery efforts.
Keyword Centipede venom
Multi-domain transcripts
MALDI imaging

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Created: Thu, 20 Feb 2014, 16:03:31 EST by Eivind Undheim on behalf of Scholarly Communication and Digitisation Service