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Article Dans Une Revue Proceedings of the National Academy of Sciences of the United States of America Année : 2020

Australian funnel-web spiders evolved human-lethal δ-hexatoxins for defense against vertebrate predators

Résumé

Australian funnel-web spiders are infamous for causing human fatalities, which are induced by venom peptides known as δ-hexatoxins (δ-HXTXs). Humans and other primates did not feature in the prey or predator spectrum during evolution of these spiders, and consequently the primate lethality of δ-HXTXs remains enigmatic. Funnel-web envenomations are mostly inflicted by male spiders that wander from their burrow in search of females during the mating season, which suggests a role for δ-HXTXs in self-defense since male spiders rarely feed during this period. Although 35 species of Australian funnel-web spiders have been described, only nine δ-HXTXs from four species have been characterized, resulting in a lack of understanding of the ecological roles and molecular evolution of δ-HXTXs. Here, by profiling venom-gland transcriptomes of 10 funnel-web species, we report 22 δ-HXTXs. Phylogenetic and evolutionary assessments reveal a 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 from the Sydney funnel-web spider Atrax robustus , induces pain in mice by inhibiting inactivation of voltage-gated sodium (Na V ) channels involved in nociceptive signaling. δ-HXTX-Ar1a also inhibited inactivation of cockroach Na V channels and was insecticidal to sheep blowflies. Considering their algogenic effects in mice, potent insecticidal effects, and high levels of sequence conservation, we propose that the δ-HXTXs were repurposed from an initial insecticidal predatory function to a role in defending against nonhuman vertebrate predators by male spiders, with their lethal effects on humans being an unfortunate evolutionary coincidence.

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Dates et versions

hal-03440284 , version 1 (22-11-2021)

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Citer

Volker Herzig, Kartik Sunagar, David Wilson, Sandy Pineda, Mathilde Israel, et al.. Australian funnel-web spiders evolved human-lethal δ-hexatoxins for defense against vertebrate predators. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117 (40), pp.24920-24928. ⟨10.1073/pnas.2004516117⟩. ⟨hal-03440284⟩
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