Clawing through Evolution: Toxin Diversification and Convergence in the Ancient Lineage Chilopoda (Centipedes)

Undheim, Eivind A. B.; Jones, Alun; Clauser, Karl R.; Holland, John W.; Pineda, Sandy S.; King, Glenn F.; Fry, Bryan G.

doi:10.1093/molbev/msu162

Cited by 87 publications

(181 citation statements)

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“…The density of pores is also higher in S. morsitans, resulting in a much larger overall number of secretory units in the gland. These results agree with those from the comparative study by Dugon and Arthur (20), and support the hypothesis that the high morphological complexity of scolopendrid venom glands may be unique among centipedes (19).…”

Section: Resultssupporting

confidence: 90%

“…The relatively higher abundance of detectable ions in the scolopendrid venom glands (19) therefore means that suppression effects are likely to be greater than in T. longicornis, leading to apparently less-diverse mass spectra.…”

Section: Resultsmentioning

confidence: 99%

“…Thus, the centipede venom apparatus should be a useful model system for gaining insight into the impact of morphological constraints on venom evolution. Surprisingly, despite lacking the formidable physical weaponry of scolopendrid centipedes, scutigeromorph venoms appear to be relatively noncomplex (19). The venom of a single scolopendrid species can contain over 30 distinct toxin families, often more than half of which are cysteine-rich peptides smaller than 10 kDa.…”

Section: Significancementioning

confidence: 99%

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Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

Undheim

Hamilton

Kurniawan³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Venom represents one of the most extreme manifestations of a chemical arms race. Venoms are complex biochemical arsenals, often containing hundreds to thousands of unique protein toxins. Despite their utility for prey capture, venoms are energetically expensive commodities, and consequently it is hypothesized that venom complexity is inversely related to the capacity of a venomous animal to physically subdue prey. Centipedes, one of the oldest yet least-studied venomous lineages, appear to defy this rule. Although scutigeromorph centipedes produce less complex venom than those secreted by scolopendrid centipedes, they appear to rely heavily on venom for prey capture. We show that the venom glands are large and well developed in both scutigerid and scolopendrid species, but that scutigerid forcipules lack the adaptations that allow scolopendrids to inflict physical damage on prey and predators. Moreover, we reveal that scolopendrid venom glands have evolved to accommodate a much larger number of secretory cells and, by using imaging mass spectrometry, we demonstrate that toxin production is heterogeneous across these secretory units. We propose that the differences in venom complexity between centipede orders are largely a result of morphological restrictions of the venom gland, and consequently there is a strong correlation between the morphological and biochemical complexity of this unique venom system. The current data add to the growing body of evidence that toxins are not expressed in a spatially homogenous manner within venom glands, and they suggest that the link between ecology and toxin evolution is more complex than previously thought. venom evolution | venom-gland morphology | centipede | mass spectrometry imaging | venom optimization hypothesis

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Section: Resultssupporting

confidence: 90%

Section: Resultsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

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Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

Undheim

Hamilton

Kurniawan³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…fleckeri haemolysin toxins CfTX-A (UniProt: T1PRE3) and CfTX-B (UniProt: T1PQV6) and potent cardiotoxic toxin CfTX-1 (UniProt: A7L035) [13] [228], centipedes [99], and the jellyfish Stomolophus meleagris [12]. These proteins are thought to be responsible for degrading the extracellular matrix, thereby facilitating the diffusion of other venom components to their molecular targets.…”

Section: Comparative Proteomic Analyses and Identified Proteinsmentioning

confidence: 99%

“…Most venomics studies to date have been using whole venom (shotgun) proteomics, 2-D fractionation (ion-exchange followed by HPLC) and SDS-PAGE electrophoresis in order to discover the maximal number of proteins in a sample [14,91,99,241].…”

Section: Transcriptomic and Proteomic Analyses 41 Introductionmentioning

confidence: 99%

Evolution and diversification of the cnidarian venom system

Jouiaei¹

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The phylum Cnidaria (corals, sea pens, sea anemones, jellyfish and hydroids) is the oldest venomous animal lineage (~750 million years old), making it an ideal phylum to understand the origin and diversification of venom. Cnidarians are characterised by specialised cellular structures called cnidae, which they utilise to inject mixtures of bioactive compounds or venom for predation and defence. In recent years cnidarian venoms have begun to be investigated as a potential source of novel bioactive therapeutics. However, in comparison with several venomous lineages that are relatively younger, such as snakes, cone snails and spiders, the diversification and molecular evolutionary regimes of toxins encoded by these fascinating and ancient animals remain poorly understood.The first experimental part of this thesis (Chapter 2) is comprised of the phylogenetic and molecular evolutionary histories of pharmacologically characterised cnidarian toxin families. These include 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 small cysteine-rich peptides (SCRiPs). Our analyses show that most cnidarian toxins remain conserved under the strong influence of negative selection. A deeper analysis of the molecular evolutionary histories of neurotoxins demonstrates 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 also identify a few functionally important sites in other classes of neurotoxins and pore-forming toxins that experienced episodic adaptation. In addition, we describe the first family of neurotoxic peptides (SCRiPs) in reef-building corals, Acropora millepora, that are likely involved in the envenoming function.The third chapter describes the development of a novel venom extraction technique which is rapid, repeatable and cost effective. This technique involves using ethanol to both induce cnidae discharge and to recover venom contents in one step. Our model species is the notorious Australian box jellyfish (Chironex fleckeri) which has a notable impact on public health. By using the complementary approaches of transcriptomics, proteomics, mass spectrometry, histology, and scanning electron microscopy, this study compares the proteome profile of the new ethanol recovery based method to a previously reported protocol, based upon density purified intact cnidae and pressure induced disruption. This work not only results in the expansion of identified Australian box jellyfish venom components but also illustrates that ethanol extraction method could greatly augment future cnidarian venom proteomics research efforts.The forth chapter is constituted by previously described venom extraction technique, ethanolinduced discharge of cnidae, to rapidly and efficiently characterise venom components of the Jelly Blubber or Blue Blubber Jellyfish, Catostylus mosaicus. By us...

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Toxin structures as evolutionary tools: Using conserved 3D folds to study the evolution of rapidly evolving peptides

2016

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Three-dimensional (3D) structures have been used to explore the evolution of proteins for decades, yet they have rarely been utilized to study the molecular evolution of peptides. Here, we highlight areas in which 3D structures can be particularly useful for studying the molecular evolution of peptide toxins. Although we focus our discussion on animal toxins, including one of the most widespread disulfide-rich peptide folds known, the inhibitor cystine knot, our conclusions should be widely applicable to studies of the evolution of disulfide-constrained peptides. We show that conserved 3D folds can be used to identify evolutionary links and test hypotheses regarding the evolutionary origin of peptides with extremely low sequence identity; construct accurate multiple sequence alignments; and better understand the evolutionary forces that drive the molecular evolution of peptides. Also watch the video abstract.

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Clawing through Evolution: Toxin Diversification and Convergence in the Ancient Lineage Chilopoda (Centipedes)

Cited by 87 publications

References 100 publications

Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

Evolution and diversification of the cnidarian venom system

Toxin structures as evolutionary tools: Using conserved 3D folds to study the evolution of rapidly evolving peptides

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