Myoinhibitory peptide regulates feeding in the marine annelidPlatynereis

Abstract

Background: During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. How larvae regulate changes in feeding during this life-cycle transition is not well understood. Neuropeptides are known to regulate several aspects of feeding, such as food search, ingestion and digestion. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. The conserved neuropeptide myoinhibitory peptide (MIP) is a key regulator of larval settlement behavior in Platynereis. Whether MIP also regulates the initiation of feeding, another aspect of the pelagic-to-benthic transition in Platynereis, is currently unknown.

High diversity in neuropeptide immunoreactivity patterns among three closely related species of Dinophilidae (Annelida)

“…To further characterize nervous system anatomy using cell‐specific markers, we decided to also use neuropeptide antibodies. Several antibodies recognizing annelid neuropeptides have been developed for the nereid annelid Platynereis dumerilii (Conzelmann et al, ; Conzelmann & Jékely, ; Shahidi et al, 2015; Williams et al, ; Williams et al, ). To check the conservation of the Platynereis peptides in the three species we searched in the available transcriptomes of D. gyrociliatus (SRX2030658, Kerbl et al, ), D. taeniatus (SRX1025580, Andrade et al ) and T. axi (SRR2014693, Struck et al ), where we identified homologs for several Platynereis proneuropeptides in at least one of the species (Table ).…”

“…The specificity of these antibodies against AT, FVamide (FV), and MIP was tested by morpholino gene knockdown in larvae of P. dumerilii (Shahidi, Williams, Conzelmann, Asadulina, Verasztó, Jasek, Bezares‐Calderón, Jékely, & Calabrese, 2015; Williams et al, ), and the specificity of antibodies against calcitonin (CT), DLamide (DL), excitatory peptide (EP), FLamide (FL), FV, FVRIamide (FVRI), MLD/pedal peptide (MLD), RGW, RNamide/sCAP (sCAP), SIFamide (SIF), and VT was tested by whole mount in situ hybridization in larvae (Tables , , Jékely, ; Conzelmann et al, ; Asadulina, Panzera, Verasztó, Liebig, & Jékely, ; Conzelmann & Jékely, ; Shahidi et al, 2015; Williams et al, ).…”

“…Within annelids, Platynereis dumerilii (Audouin & Milne‐Edwards, 1834) and to some extend also Capitella teleta Blake, Grassle & Eckelbarger, 2009 have been established as model animals, and their neurogenesis and detailed anatomy have been reconstructed (Meyer & Seaver, ; Fischer, Henrich, & Arendt, ; Meyer et al, ) as well as the neural circuits related to, for example, vision and feeding (Conzelmann et al, ; Randel et al, ; Williams, Conzelmann, & Jékely, ). These neural circuits are repeatedly shown to feature cells with specific neuropeptide profiles (Wilgren, Reuter, & Gustafsson, ; Pape, Juengling, Seidenbecher, Lesting, & Reinscheid, ; Conzelmann et al, ; Randel et al, ; Schoofs & Beets, ), thereby indicating that these molecules and their interactions play a major role in orchestrating behavior (Argiolas, ; Kristan, Calabrese, & Friesen, ; Nylander & Roman, ; Giulianini & Edomi, ).…”

“…Fewer members of the invertebrate sister group, Spiralia, are studied for the detailed functions of individual neuropeptides (Stent, Thompson, & Calabrese, ; Lloyd, Kupfermann, & Weiss, ; Sweedler et al, ; Zhen & Samuel, ). Expression of neuropeptides such as the myoinhibitory protein (MIP) (e.g., Conzelmann et al, , Williams et al, ) seems to be limited to clearly defined regions in the nervous system of the tested Spiralians, whereby the inclusion of more specific neural markers for the characterization of nervous systems may complement the patterns observed with broadly expressed neurotransmitter markers such as FMRFamide (Diaz‐Miranda, de Motta, & García‐Arrarás, ; Orchard & Lange, ) or serotonin (Miron & Anctil, ; Barlow & Truman, ; Kerbl et al, ; Schwaha & Wanninger, ; Bekkouche & Worsaae, ; Kerbl et al, ).…”

Dual signaling of Wamide myoinhibitory peptides through a peptide‐gated channel and a GPCR in Platynereis

“…A comprehensive complement of neuropeptides has been described for this species, consisting of 100 proneuropeptide genes (12). Several of these neuropeptides have been mapped to the nervous system and have been studied functionally (13)(14)(15)(16)(17). Furthermore, .20 different neuropeptide and monoamine GPCRs have been experimentally identified in Platynereis, including the founding members of several major bilaterian neuropeptide-receptor families (achatin, FMRFamide, RGWamide, FLamide, and elevenin receptors) and the first invertebrate adrenergic receptors (17)(18)(19).…”