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Australian Funnel-Web Spiders Evolved Human-Lethal Δ-Hexatoxins for Defense Against Vertebrate Predators

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Australian Funnel-Web Spiders Evolved Human-Lethal Δ-Hexatoxins for Defense Against Vertebrate Predators Australian funnel-web spiders evolved human-lethal δ-hexatoxins for defense against vertebrate predators Volker Herziga,b,1,2, Kartik Sunagarc,1, David T. R. Wilsond,1, Sandy S. Pinedaa,e,1, Mathilde R. Israela, Sebastien Dutertref, Brianna Sollod McFarlandg, Eivind A. B. Undheima,h,i, Wayne C. Hodgsonj, Paul F. Alewooda, Richard J. Lewisa, Frank Bosmansk, Irina Vettera,l, Glenn F. Kinga,2, and Bryan G. Frym,2 aInstitute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; bGeneCology Research Centre, School of Science and Engineering, University of the Sunshine Coast, Sippy Downs, QLD 4556, Australia; cEvolutionary Venomics Lab, Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560012, India; dCentre for Molecular Therapeutics, Australian Institute of Tropical Health and Medicine, James Cook University, Smithfield, QLD 4878, Australia; eBrain and Mind Centre, University of Sydney, Camperdown, NSW 2052, Australia; fInstitut des Biomolécules Max Mousseron, UMR 5247, Université Montpellier, CNRS, 34095 Montpellier Cedex 5, France; gSollod Scientific Analysis, Timnath, CO 80547; hCentre for Advanced Imaging, The University of Queensland, St Lucia, QLD 4072, Australia; iCentre for Ecology and Evolutionary Synthesis, Department of Biosciences, University of Oslo, 0316 Oslo, Norway; jMonash Venom Group, Department of Pharmacology, Monash University, Clayton, VIC 3800, Australia; kBasic and Applied Medical Sciences Department, Faculty of Medicine, Ghent University, 9000 Ghent, Belgium; lSchool of Pharmacy, The University of Queensland, Woolloongabba, QLD 4102, Australia; and mVenom Evolution Laboratory, School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved August 9, 2020 (received for review March 10, 2020) Australian funnel-web spiders are infamous for causing human δ-HXTXs and δ-AOTX comprise 42 to 44 residues and con- fatalities, which are induced by venom peptides known as tain four disulfide bonds, three of which are arranged in an in- δ-hexatoxins (δ-HXTXs). Humans and other primates did not fea- hibitor cystine knot (ICK) motif (8, 9). δ-HXTXs slow the ture in the prey or predator spectrum during evolution of these inactivation of vertebrate tetrodotoxin-sensitive voltage-gated δ spiders, and consequently the primate lethality of -HXTXs re- sodium (NaV) channels and insect NaV channels by binding to mains enigmatic. Funnel-web envenomations are mostly inflicted the voltage sensor in channel domain IV (10, 11). In human bite by male spiders that wander from their burrow in search of fe- victims, δ-HXTXs cause disturbances in respiration, blood males during the mating season, which suggests a role for pressure, and heart rate, followed by severe hypotension. With- δ-HXTXs in self-defense since male spiders rarely feed during this out treatment with commercial antivenom (5), fatalities can oc- EVOLUTION period. Although 35 species of Australian funnel-web spiders have cur by respiratory and circulatory failure within a few hours of δ been described, only nine -HXTXs from four species have been the bite (12). Interestingly, in striking contrast to humans and characterized, resulting in a lack of understanding of the ecologi- other primates, some vertebrates such as dogs and cats are in- δ cal roles and molecular evolution of -HXTXs. Here, by profiling sensitive to funnel-web envenomation (13). venom-gland transcriptomes of 10 funnel-web species, we report δ Humans did not feature in the prey or predator spectrum 22 -HXTXs. Phylogenetic and evolutionary assessments reveal a during evolution of funnel-web spiders, as primates were not remarkable sequence conservation of δ-HXTXs despite their deep evolutionary origin within funnel-web spiders, consistent with a defensive role. We demonstrate that δ-HXTX-Ar1a, the lethal toxin Significance from the Sydney funnel-web spider Atrax robustus, induces pain in mice by inhibiting inactivation of voltage-gated sodium (NaV) The venom of Australian funnel-web spiders contains channels involved in nociceptive signaling. δ-HXTX-Ar1a also δ-hexatoxins (δ-HXTXs) that exert fatal neurotoxic effects in inhibited inactivation of cockroach NaV channels and was insecti- humans by inhibiting inactivation of voltage-gated sodium cidal to sheep blowflies. Considering their algogenic effects in channels, but their precise ecological role remains unclear. Se- mice, potent insecticidal effects, and high levels of sequence con- quencing of venom-gland transcriptomes from 10 funnel-web servation, we propose that the δ-HXTXs were repurposed from an species uncovered 22 δ-HXTXs. Evolutionary analysis revealed initial insecticidal predatory function to a role in defending against extreme conservation of these toxins, despite their ancient nonhuman vertebrate predators by male spiders, with their lethal origin. We isolated the lethal δ-HXTX from venom of the Syd- effects on humans being an unfortunate evolutionary coincidence. ney funnel-web spider and showed that it induces pain in mice, suggesting a role in predator deterrence. Although humans are venom | evolution | spider not the target of δ-HXTXs, these toxins likely evolved to deter vertebrate predators commonly encountered by these spiders, such as bandicoots, birds, and lizards. Thus, the lethal potency espite their fearsome reputation, only a few species of spi- of δ-HXTXs against humans is an unfortunate evolutionary ders can cause death or serious harm to humans (1). An D coincidence. infamous exception is the Australian funnel-web spider, arguably ’ the world s deadliest spider (2). These spiders produce extraor- Author contributions: V.H. and B.G.F. designed research; V.H., K.S., D.T.R.W., S.S.P., M.R.I., dinarily complex venoms, with each venom containing up to S.D., B.S.M., E.A.B.U., W.C.H., P.F.A., R.J.L., F.B., I.V., and G.F.K. performed research; V.H., several thousand peptide toxins (3, 4). Despite this chemical K.S., D.T.R.W., S.S.P., M.R.I., S.D., B.S.M., E.A.B.U., W.C.H., P.F.A., R.J.L., F.B., I.V., G.F.K., and δ B.G.F. analyzed data; and V.H., K.S., D.T.R.W., S.S.P., M.R.I., S.D., B.S.M., E.A.B.U., W.C.H., complexity, a single family of toxins known as the -hexatoxins P.F.A., R.J.L., F.B., I.V., G.F.K., and B.G.F. wrote the paper. δ ( -HXTXs) is responsible for the human envenomation syn- The authors declare no competing interest. drome (5). There are currently 35 described species of Austra- This article is a PNAS Direct Submission. lian funnel-web spiders and 38 species of related non-Australian Published under the PNAS license. funnel-web spiders in the genus Macrothele, but to date only 12 δ- 1V.H., K.S., D.T.R.W., and S.S.P. contributed equally to this work. HXTX sequences have been reported from six species within this 2 δ δ To whom correspondence may be addressed. Email: [email protected], glenn.king@ broad clade. A homologous -actinopoditoxin ( -AOTX) is pre- imb.uq.edu.au, or [email protected]. sent in the venom of the related Australian mouse spider Mis- This article contains supporting information online at https://www.pnas.org/lookup/suppl/ sulena bradleyi (6), which can cause serious human envenomations doi:10.1073/pnas.2004516117/-/DCSupplemental. with symptoms resembling those from funnel-web spider bites (7). www.pnas.org/cgi/doi/10.1073/pnas.2004516117 PNAS Latest Articles | 1of9 Downloaded by guest on September 30, 2021 Fig. 1. Phylogenetic reconstruction of δ-HXTXs. Tree representing the phylogenetic history of δ-HXTXs as estimated by maximum-likelihood inference. The thickness of branches corresponds to node supports (thick branch, bootstrap ≥ 75; thin branch, bootstrap < 75), and various species are presented in distinct colors. The cysteine pattern (black lines) and activities (red lines) are annotated (Right). Fly and mouse icons indicate insecticidal and vertebrate activity, respectively. The underscore sequence numbers refer to the unique preprotoxin nomenclature used in the ArachnoServer database (23). present 150 to 200 million y ago (MYA) when these spiders (15, 16), which might suggest a role in prey capture. However, in originated (14). Thus, the underlying reason for the peculiar some species, these toxins are secreted in very low abundance in susceptibility of humans to δ-HXTXs and the ecological role of the venoms of female spiders and immature males, consistent these toxins remain enigmatic. The δ-HXTXs are insecticidal with the fact that only sexually mature male spiders cause severe 2of9 | www.pnas.org/cgi/doi/10.1073/pnas.2004516117 Herzig et al. Downloaded by guest on September 30, 2021 or lethal human envenomations (17). Moreover, it is hard to In the current study, we identified 22 δ-HXTX sequences from reconcile a role for these toxins in predation given that sexually 10 species of Australian funnel-web spiders, and evaluated their mature males, in whose venom the toxins are most abundant, molecular evolution, phylogenetic histories, insecticidal activity, rarely feed during the mating season. Rather, the fact that adult and potency against human NaV channels involved in pain sig- males leave the safety of their burrows to search for female naling. Taken together, our data provide strong evidence that the spiders (2), making them more susceptible to predators, suggests δ-HXTXs were recruited by funnel-web spiders as a weapon to a role for the δ-HXTXs in predator deterrence. A well- deter vertebrate predators, and that their lethal effects on hu- documented strategy for defensive toxins is to induce pain mans is an unfortunate evolutionary coincidence. (18–20), and pain is a common symptom following funnel-web envenomation (2, 17). Consistent with the idea that the Results δ-HXTXs serve a defensive role by inducing pain in vertebrate δ-HXTX Sequences.
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