The development of early pioneer neurons in the annelid Malacoceros fuliginosus

Abstract

Background Nervous system development is an interplay of many processes: the formation of individual neurons, which depends on whole-body and local patterning processes, and the coordinated growth of neurites and synapse formation. While knowledge of neural patterning in several animal groups is increasing, data on pioneer neurons that create the early axonal scaffold are scarce. Here we studied the first steps of nervous system development in the annelid Malacoceros fuliginosus . Results Here, we performed a dense expression profiling of a broad set of neural genes. We found that SoxB expression begins at 4 hours postfertilization, and shortly later, the neuronal progenitors can be identified at the anterior and the posterior pole by the transient and dynamic expression of proneural genes. At 9 hpf, the first neuronal cells start differentiating, and we provide a detailed description of axonal outgrowth of the pioneer neurons that create the primary neuronal scaffold. Tracing back the clonal origin of the ventral nerve cord pioneer neuron revealed that it is a descendant of the blastomere 2d (2d 221 ), which after 7 cleavages starts expressing Neurogenin , Achaete-Scute and NeuroD . Conclusions We propose that an anterior and posterior origin of the nervous system is ancestral in annelids. The specification of the relevant neurons starts very early and we suggest that closer examination of the first pioneer neurons will be valuable in better understanding of nervous system development in spirally cleaving animals, to determine the potential role of cell-intrinsic properties in neuronal specification and to resolve the evolution of nervous systems.

Comparative analysis defines a broader FMRFamide-gated sodium channel family and determinants of neuropeptide sensitivity

“…To investigate the presence of FMRFa sensitive channels throughout the metazoans, DEG/ENaC amino acid sequences were sought from four mollusks ( Crassostrea gigas, Octopus bimaculoides, Pinctada fucata, Lottia gigantea ), four cnidarians ( Aurelia aurita, Hydra vulgaris, Nematostella vectensis, Stylophora pistillata ), four annelids ( Capitella teleta, Platynereis dumerili, Malacoceros fuliginosus, Helobdella robusta ), one phoronid ( Phoronis australis ), one brachiopod ( Lingula anatina ), one nemertean ( Notospermus geniculatus ), one rotifer ( Branchionus plicatilis ), one platyhelminth ( Macrostomum lignano ), one arthropod ( Araneus ventricosus ), one priapulid ( Priapulus caudatus ), two chordates ( Branchiostoma belcheri, Homo sapiens ), two echinoderms ( Acanthaster planci, Strongylocentrotus purpuratus ), two poriferans ( Amphimedon queenslandica, Oscarella carmela ), one ctenophore ( Mnemiopsis leidyi ), one hemichordate ( Ptychodera flava ). Sequences were obtained through BlastP using the Aplysia kurodai FaNaC amino acid sequence (NCBI BAE07082.1) in JGI Capca1 genome ( Capitella teleta , https://mycocosm.jgi.doe.gov/pages/blast-query.jsf?db=Capca1 (37)), OIST Marine Genomics Unit ( P. fucata, P. australis, N. geniculatus, A. aurita , https://marinegenomics.oist.jp/gallery), Macrostomum lignano genome initiative ( M. lignano , http://www.macgenome.org/blast/index.html), Compagen Japan ( O. carmela , http://203.181.243.155/blast.html), our own Malacoceros fuliginosus transcriptome resources (38), or NCBI (for all others, https://blast.ncbi.nlm.nih.gov). After an initial alignment using MAFFT v 7.450 in Geneious Prime (Geneious), removal of >90% identical, redundant sequences and removal of obviously incomplete sequences, sequences were re-aligned with MAFFT and poor-aligning segments and sequences larger than 1000 amino acids or shorter than 300 amino acids were removed.…”

“…/mycocosm.jgi.doe.gov/pages/blast-query.jsf?db=Capca1(37)), OIST Marine Genomics Unit (P. fucata, P. australis, N. geniculatus, A. aurita, https://marinegenomics.oist.jp/gallery), http://203.181.243.155/blast.html), our own Malacoceros fuliginosus transcriptome resources(38), or NCBI (for all others, https://blast.ncbi.nlm.nih.gov). After an initial alignment using MAFFT v 7.450 in Geneious Prime (Geneious), removal of >90% identical, redundant sequences and removal of obviously incomplete sequences, sequences were realigned with MAFFT and poor-aligning segments and sequences larger than 1000 amino acids or shorter than 300 amino acids were removed.…”

The visual pigment xenopsin is widespread in protostome eyes and impacts the view on eye evolution

“…For studies on M. fuliginosus, we used transcriptomic resources prepared in an earlier study ( Kumar et al, 2020 ) from pooled larvae of several stages. For T. inopinata, we performed RNA-seq and de novo transcriptome assembly.…”

Palps across the tree – the neuronal innervation and development of sensory head appendages in Annelida

“…For more details on culturing and artificial fertilization for Magelona mirabilis we refer to Beckers et al (2019a). For details about the culture of Malacoceros fuliginosus please see Kumar (2019) and Kumar et al (2020).…”