Functional analysis of kainate receptors in the spider Argiope bruennichi reveals glutamatergic signalling in both central and peripheral nervous systems

Arthropod neurobiology has been studied overwhelmingly in insects, leaving the molecular basis of sensory systems in non-insect arthropods poorly understood; addressing this gap is necessary to enrich our knowledge of these understudied groups. Spiders possess sensory systems distinct from insects, with synapses in peripheral sensory nerves, positioning them as an ideal model for investigating peripheral neurotransmitter signalling and arthropod sensory diversity. Here, we investigated ionotropic glutamate receptors (iGluRs) in the wasp spider Argiope bruennichi . Classic iGluRs (NMDA, AMPA and kainate receptors) mediate most excitatory synaptic transmission via the neurotransmitter glutamate in the central nervous system of both vertebrates and invertebrates, while the variant ionotropic receptors (IRs) perform diverse sensory roles in insects. However, the function of iGluRs/IRs in other arthropods remains largely unexplored. We identified two kainate receptors, AbruKAR1 and AbruKAR2, which are highly abundant and broadly expressed across the central and peripheral nervous systems of A. bruennichi . Heterologous expression in Xenopus oocytes revealed that these two receptors form a functional heteromeric complex, selectively activated by kainate receptor agonists. AbruKAR1/AbruKAR2 share common functional properties with insect kainate receptors, including Ca 2+ permeability and rapid desensitization blocked by Concanavalin A. However, they show independence from auxiliary proteins and much higher glutamate sensitivity compared to insects. Our research expands the current knowledge of iGluR function and evolution, suggesting diverse expression patterns and physiological roles for arthropod kainate receptors. It provides compelling evidence for a sensitive and broadly distributed glutamatergic signalling system in spiders, which may play important roles in modulating peripheral sensory neurons. • The first functional characterization of iGluRs in a non-insect arthropod. • Two kainate-type iGluRs of the wasp spider form a selective heteromeric assembly. • The highly sensitive glutamatergic signalling in both the peripheral and central circuits. • Kainate receptors may play a broad role in modulating peripheral sensory neurons. • Spiders as an insightful model for studying the architecture of non-canonical sensory systems.