Abstract
The allatostatins (ASTs), AST-A, AST-B and AST-C, have mainly been investigated in insects. They are a large group of small pleotropic alloregulatory neuropeptides that are unrelated in sequence and activate receptors of the rhodopsin G-protein coupled receptor family (GPCRs). The characteristics and functions of the homologue systems in the molluscs (Buccalin, MIP and AST-C-like), the second most diverse group of protostomes after the arthropods, and of high interest for evolutionary studies due to their less rearranged genomes remains to be explored. In the present study their evolution is deciphered in molluscs and putative functions assigned in bivalves through meta-analysis of transcriptomes and experiments. Homologues of the three arthropod AST-type peptide precursors were identified in molluscs and produce a larger number of mature peptides than in insects. The number of putative receptors were also distinct across mollusc species due to lineage and species-specific duplications. Our evolutionary analysis of the receptors identified for the first time in a mollusc, the cephalopod, GALR-like genes, which challenges the accepted paradigm that AST-AR/buccalin-Rs are the orthologues of vertebrate GALRs in protostomes. Tissue transcriptomes revealed the peptides, and their putative receptors have a widespread distribution in bivalves and in the bivalve Mytilus galloprovincialis, elements of the three peptide-receptor systems are highly abundant in the mantle an innate immune barrier tissue. Exposure of M. galloprovincialis to lipopolysaccharide or a marine pathogenic bacterium, Vibrio harveyi, provoked significant modifications in the expression of genes of the peptide precursor and receptors of the AST-C-like system in the mantle suggesting involvement in the immune response. Overall, our study reveals that homologues of the arthropod AST-systems in molluscs are potentially more complex due to the greater number of putative mature peptides and receptor genes. In bivalves they have a broad and varying tissue distribution and abundance, and the elements of the AST-C-like family may have a putative function in the immune response.
Highlights
Molluscs are the second most diverse animal group after the insects and belong to the speciose Lophotrochozoan clade
In molluscs the sequence orthologues of the arthropod allatostatin A (AST-A) are known as buccalin and in annelids the orthologues of the arthropod AST-B/myoinhibiting peptides (MIPs) are known as MIP
The mature peptides and receptor members (Buccalin, MIP and AST-C-like) were distinct across mollusc species, and this suggests that the AST families may be as complex as the neuropeptide system described in insects and other arthropods
Summary
Molluscs are the second most diverse animal group after the insects and belong to the speciose Lophotrochozoan clade. Unlike the more popular protostome models of the nematodes and insects that have substantial genome rearrangements and gene loss [1,2,3,4], the molluscs have a more similar genome organisation and gene repertoire to deuterostomes Their success, exquisite diversity in form and function and less rearranged genomes makes the molluscs of particular interest for evolutionary studies directed at deciphering the evolution, diversification and role of neuroendocrine factors [1, 5]. The ASTs are best studied in insects and despite the relatively low gene sequence conservation between the AST families their function and distribution has been conserved This provides an interesting opportunity to assess if functional constraints have shaped AST evolution in the same way across the protostomes
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