Abstract

The biogenic amines octopamine (OA), tyramine (TA), dopamine (DA), serotonin (5-HT), and histamine (HA) affect diverse physiological and behavioral processes in invertebrates, but recent findings indicate that an additional adrenergic system exists in at least some invertebrates. Transcriptome analysis has made it possible to identify biogenic amine receptor genes in a wide variety of species whose genomes have not yet been sequenced. This approach provides new sequences for research into the evolutionary history of biogenic amine receptors and allows them to be studied in experimentally accessible animal models. The Central American Wandering spider, Cupiennius salei, is an experimental model for neurophysiological, developmental and behavioral research. We identified ten different biogenic amine receptors in C. salei transcriptomes. Phylogenetic analysis indicated that, in addition to the typical receptors for OA, TA, DA, and 5-HT in protostome invertebrates, spiders also have α1- and α2-adrenergic receptors, but lack TAR2 receptors and one invertebrate specific DA receptor type. In situ hybridization revealed four types of biogenic amine receptors expressed in C. salei mechanosensory neurons. We used intracellular electrophysiological experiments and pharmacological tools to determine how each receptor type contributes to modulation of these neurons. We show that arachnids have similar groups of biogenic amine receptors to other protostome invertebrates, but they lack two clades. We also clarify that arachnids and many other invertebrates have both α1- and α2-adrenergic, likely OA receptors. Our results indicate that in addition to an OAβ-receptor that regulates rapid and large changes in sensitivity via a Gs-protein activating a cAMP mediated pathway, the C. salei mechanosensory neurons have a constitutively active TAR1 and/or α2-adrenergic receptor type that adjusts the baseline sensitivity to a level appropriate for the behavioral state of the animal by a Gq-protein that mobilizes Ca2+.

Highlights

  • The biogenic amines histamine (HA), dopamine (DA), and serotonin (5-HT) are common neurotransmitters in both vertebrates and invertebrates, but adrenergic signaling has been considered absent in protostome invertebrates, where monoamine octopamine (OA) and its precursor tyramine (TA) have replaced noradrenaline and adrenaline

  • The relative abundance of transcribed mRNA for each putative biogenic amine receptor sequence was estimated by searching the transcriptome data for matches to the main open reading frame as explained previously in detail (French, 2012; Torkkeli et al, 2015)

  • All ten sequences were found in both tissues, and generally in similar amounts, but the relative abundances of some (CsTAR1, CsDAR2A, and CsDAR2B) were higher in the Central Nervous System (CNS) than in the hypodermis while other sequences were more abundant in the hypodermis (CsOARβA and CsOARα)

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Summary

Introduction

The biogenic amines histamine (HA), dopamine (DA), and serotonin (5-HT) are common neurotransmitters in both vertebrates and invertebrates, but adrenergic signaling has been considered absent in protostome invertebrates, where monoamine octopamine (OA) and its precursor tyramine (TA) have replaced noradrenaline and adrenaline (Roeder, 2005; Lange, 2009; Spider Biogenic Amine ReceptorsOhta and Ozoe, 2014; Blenau et al, 2017a,b). (2) β-adrenergic-like OA receptors (OARβ), acting only on Gs proteins to stimulate cAMP production (Balfanz et al, 2005; Evans and Maqueira, 2005; Verlinden et al, 2010; Ohta and Ozoe, 2014). Two other receptor types in many arthropods have their highest affinity to TA: (1) TAR1 receptors are structurally closest to vertebrate α2-adrenergic receptors, activated by both TA and OA (Lange, 2009) They signal by inhibiting cAMP production via Gi proteins and/or activate Gq proteins to elevate [Ca2+] (Evans and Maqueira, 2005). When expressed in cell lines, some of these receptors respond to adrenaline and/or noradrenaline suggesting that the evolutionary history of adrenergic signaling may not have been as direct as previously thought (Bauknecht and Jekely, 2017)

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