Proteomics and Deep Sequencing Comparison of Seasonally Active Venom Glands in the Platypus Reveals Novel Venom Peptides and Distinct Expression Profiles

Wong, Emily S.; Morgenstern, David; Mofiz, Ehtesham; Gombert, Sara; Morris, Katrina M.; Temple-Smith, Peter; Renfree, Marilyn B.; Whittington, Camilla M.; King, Glenn F.; Warren, Welsey C; Papenfuss, Anthony T.; Belov, Katherine

doi:10.1074/mcp.m112.017491

Cited by 40 publications

(37 citation statements)

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“…However, our understanding of the factors shaping venom evolution, and our ability to repurpose venom toxins for biotechnological use, is limited by the current focus of research on a small number of prominent groups of venomous animals: the scorpions, spiders, snakes, and cone snails. Studies on neglected taxa (12)(13)(14)(15)(16) are essential to gain a more general understanding of how venom systems evolve and how venom evolution is influenced by factors such as geographical, trophic, and morphological constraints.…”

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confidence: 99%

Melt With This Kiss: Paralyzing and Liquefying Venom of The Assassin Bug Pristhesancus plagipennis (Hemiptera: Reduviidae)

Walker

Madio

Jin

et al. 2017

Molecular & Cellular Proteomics

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Assassin bugs (Hemiptera: Heteroptera: Reduviidae) are venomous insects, most of which prey on invertebrates. Assassin bug venom has features in common with venoms from other animals, such as paralyzing and lethal activity when injected, and a molecular composition that includes disulfide-rich peptide neurotoxins. Uniquely, this venom also has strong liquefying activity that has been hypothesized to facilitate feeding through the narrow channel of the proboscis-a structure inherited from sapand phloem-feeding phytophagous hemipterans and adapted during the evolution of Heteroptera into a fang and feeding structure. However, further understanding of the function of assassin bug venom is impeded by the lack of proteomic studies detailing its molecular composition.By using a combined transcriptomic/proteomic approach, we show that the venom proteome of the harpactorine assassin bug Pristhesancus plagipennis includes a complex suite of >100 proteins comprising disulfide-rich peptides, CUB domain proteins, cystatins, putative cytolytic toxins, triabin-like protein, odorant-binding protein, S1 proteases, catabolic enzymes, putative nutrient-binding proteins, plus eight families of proteins without homology to characterized proteins. S1 proteases, CUB domain proteins, putative cytolytic toxins, and other novel proteins in the 10 -16-kDa mass range, were the most abundant venom components. Thus, in addition to putative neurotoxins, assassin bug venom includes a high proportion of enzymatic and cytolytic venom components likely to be well suited to tissue liquefaction. Our results also provide insight into the trophic switch to blood-feeding by the kissing bugs (Reduviidae: Triatominae). Although some protein families such as triabins occur in the venoms of both predaceous and blood-feeding reduviids, the composition of venoms produced by these two groups is revealed to differ markedly. These results provide insights into the venom evolution in the insect suborder Heteroptera. Venoms are chemical arsenals injected by one animal into another to disrupt the homeostasis of the injected animal in ways that assist predation, defense, or feeding by the injecting animal (1). Typically, venoms are composed of multiple toxins, including peptides, enzymes, and small molecules, such as polyamines, that bind to and affect the function of multiple molecular targets in the injected animal. Because of their key role governing life-or-death interactions between animals, venom toxins are subject to selection pressures that have resulted in unique evolutionary patterns such as massive duplication and accelerated evolution of toxin-encoding genes (2-5). In addition, the properties that ensure that toxins confer a fitness advantage to the animals that produce them, including high stability and potency, make them well suited for use as insecticides, therapeutics, and pharmacological tools (6 -11). However, our understanding of the factors shaping venom evolution, and our ability to repurpose venom toxins for biotechnological use, is limited ...

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confidence: 99%

Melt With This Kiss: Paralyzing and Liquefying Venom of The Assassin Bug Pristhesancus plagipennis (Hemiptera: Reduviidae)

Walker

Madio

Jin

et al. 2017

Molecular & Cellular Proteomics

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“…1087-1089Moyal, 2001, p. 204;Grant, 2007, p. 48;Whittington and Belov, 2007, pp. 57, 60;Wong et al, 2012Wong et al, , p. 1362.…”

Section: Evolutionary Backwaters and Eco-nationalismmentioning

confidence: 90%

“…58-60;Warren et al, 2008, pp. 177-180;Wong et al, 2012Wong et al, , p. 1361. Arguing that the poisons of snakes, platypuses, shrews and other venomous mammals likely emerged independently, these studies sever any putative evolutionary linkages based upon venom production as a preserved characteristic (Whittington et al, 2008, p. 991).…”

Section: Conclusion: Fluid Definitionsmentioning

confidence: 93%

A Spur to Atavism: Placing Platypus Poison

Hobbins

2015

J Hist Biol

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For over two centuries, the platypus (Ornithorhynchus anatinus) has been constructed and categorized in multiple ways. An unprecedented mélange of anatomical features and physiological functions, it long remained a systematic quandary. Nevertheless, since 1797, naturalists and biologists have pursued two recurring obsessions. Investigations into platypus reproduction and lactation have focused attention largely upon females of the species. Despite its apparent admixture of avian, reptilian and mammalian characters, the platypus was soon placed as a rudimentary mammal--primitive, naïve and harmless. This article pursues a different taxonomic trajectory, concentrating on a specifically male anatomical development: the crural spur and venom gland on the hind legs. Once the defining characteristic of both the platypus and echidna (Tachyglossus aculeatus), by 1830 this sexed spur had been largely dismissed as inactive and irrelevant. For a creature regularly depicted as a biological outlier, the systematic and evolutionary implications of platypus poison have remained largely overlooked. In Australia, however, sporadic cases of 'spiking' led to consistent homologies being remarked between the platypus crural system and the venom glands of snakes. As with its reproductive reliance upon eggs, possession of an endogenous poison suggested significant reptilian affinities, yet the platypus has rarely been classed as an advanced reptile. Indeed, ongoing uncertainty regarding the biological purpose of the male's spur has ostensibly posed a directional puzzle. As with so many of its traits, however, platypus poison has been consistently described as a redundant remnant, rather than an emergent feature indicating evolutionary advance.

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“…The impact of these technological advances is noticeable across the discipline. They enable unexpected new insights into the biology and evolution of some of the most intensely studied and best understood venom systems, such as cone snails and snakes [ 5 , 6 ], but at the same time they are dramatically accelerating research into neglected or even completely unstudied venomous taxa, such as centipedes, the platypus, polychaetes and remipede crustaceans [ 7 , 8 , 9 ].…”

Section: Introductionmentioning

confidence: 99%

“…Three recent examples illustrate how the application of new -omics techniques to neglected taxa has yielded insights at odds with our general understanding of venoms. First, the current paradigm that venom toxin genes generally result from gene duplication followed by recruitment to venom glands is not supported by insights derived from the platypus [ 9 ]. Gene duplication played a role in the origin of only 16 out of 107 platypus genes homologous to known toxin genes.…”

Section: Introductionmentioning

confidence: 99%

Quo Vadis Venomics? A Roadmap to Neglected Venomous Invertebrates

Reumont

Campbell

Jenner

2014

Toxins

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Venomics research is being revolutionized by the increased use of sensitive -omics techniques to identify venom toxins and their transcripts in both well studied and neglected venomous taxa. The study of neglected venomous taxa is necessary both for understanding the full diversity of venom systems that have evolved in the animal kingdom, and to robustly answer fundamental questions about the biology and evolution of venoms without the distorting effect that can result from the current bias introduced by some heavily studied taxa. In this review we draw the outlines of a roadmap into the diversity of poorly studied and understood venomous and putatively venomous invertebrates, which together represent tens of thousands of unique venoms. The main groups we discuss are crustaceans, flies, centipedes, non-spider and non-scorpion arachnids, annelids, molluscs, platyhelminths, nemerteans, and echinoderms. We review what is known about the morphology of the venom systems in these groups, the composition of their venoms, and the bioactivities of the venoms to provide researchers with an entry into a large and scattered literature. We conclude with a short discussion of some important methodological aspects that have come to light with the recent use of new -omics techniques in the study of venoms.

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Proteomics and Deep Sequencing Comparison of Seasonally Active Venom Glands in the Platypus Reveals Novel Venom Peptides and Distinct Expression Profiles

Cited by 40 publications

References 64 publications

Melt With This Kiss: Paralyzing and Liquefying Venom of The Assassin Bug Pristhesancus plagipennis (Hemiptera: Reduviidae)

Melt With This Kiss: Paralyzing and Liquefying Venom of The Assassin Bug Pristhesancus plagipennis (Hemiptera: Reduviidae)

A Spur to Atavism: Placing Platypus Poison

Quo Vadis Venomics? A Roadmap to Neglected Venomous Invertebrates

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