Abstract
As one of the most diverse groups of invertebrate animals, mollusks represent powerful models for neurobiological and developmental studies. Neuropeptides and peptide hormones are a heterogeneous class of signalling molecules involved in chemical communication between neurons and in neuroendocrine regulation. Here we present a fine-grained view of the molluscan neuropeptide and peptide hormone toolkit. Our results expand the distribution of several peptide families (e.g., prokineticin, insulin-related peptides, prohormone-4, LFRFamide) within Lophotrochozoa and provide evidence for an early origin of others (e.g., GNXQN/prohormone-2, neuroparsin). We identified a new peptide family broadly distributed among conchiferan mollusks, the PXRX family. We found the Wnt antagonist dickkopf1/2/4 ortholog in lophotrochozoans and nematodes and reveal that the egg-laying hormone family is a DH44 homolog restricted to gastropods. Our data demonstrate that numerous peptides evolved much earlier than previously assumed and that key signalling elements are extensively conserved among extant mollusks.
Highlights
Neuropeptides and peptide hormones constitute a heterogeneous group of evolutionarily related signalling protein molecules involved in neuro-modulation, neurotransduction, and hormonal functions[1], that commonly act via G protein-couple receptors (GPCRs)
Our analysis suggests that the evolution of the complex central nervous system (CNS) and the sophisticated behavioural repertoire of cephalopods was not paralleled by lineage-specific expansions of pNP or peptide prohormone families
Through a comparative and integrative approach using in silico protocols and sequence similarity-based clustering, a detailed overview of the minimum proneuropeptide/hormone complement of all extant class-level taxa of Mollusca was obtained
Summary
Neuropeptides and peptide hormones constitute a heterogeneous group of evolutionarily related signalling protein molecules involved in neuro-modulation, neurotransduction, and hormonal functions[1], that commonly act via G protein-couple receptors (GPCRs). Neuropeptides are secreted by neuronal cells and act on neighboring targets (cell-cell contact) whereas peptide hormones diffuse over long distances via haemolymph or blood, affecting targets far from the signalling source. The latter mechanism is controlled by the endocrine system[2]. Neuropeptides and peptide hormones are synthesized in the form of large inactive precursor molecules known as proneuropeptides (pNPs) or prohormones. They are redirected to the secretory apparatus and are further cleaved and modified to regulate homeostatic processes and distinct behaviours in animals[3]. Organism Lottia gigantea Theba pisana Deroceras reticulatum Charonia tritonis Pinctada fucata Crassostrea gigas Patinopecten yessoensis Sepia officinalis
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