Evolution of synapses and neurotransmitter systems: The divide-and-conquer model for early neural cell-type evolution

Burkhardt, Pawel; Jékely, Gáspár

doi:10.1016/j.conb.2021.11.002

Cited by 24 publications

(19 citation statements)

References 101 publications

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“…5 ). It has been assumed that the C35 cell cluster is the only cell type homologous to cnidarian and bilaterian neurons 43 . Our analysis did not detect specific conserved characteristics that distinguished C35 from other neuronal clusters (Fig.…”

Section: Discussionmentioning

confidence: 99%

Mass spectrometry of short peptides reveals common features of metazoan peptidergic neurons

et al. 2022

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The evolutionary origins of neurons remain unknown. Although recent genome data of extant early-branching animals have shown that neural genes existed in the common ancestor of animals, the physiological and genetic properties of neurons in the early evolutionary phase are still unclear. Here, we performed a mass spectrometry-based comprehensive survey of short peptides from early-branching lineages Cnidaria, Porifera and Ctenophora. We identified a number of mature ctenophore neuropeptides that are expressed in neurons associated with sensory, muscular and digestive systems. The ctenophore peptides are stored in vesicles in cell bodies and neurites, suggesting volume transmission similar to that of cnidarian and bilaterian peptidergic systems. A comparison of genetic characteristics revealed that the peptide-expressing cells of Cnidaria and Ctenophora express the vast majority of genes that have pivotal roles in maturation, secretion and degradation of neuropeptides in Bilateria. Functional analysis of neuropeptides and prediction of receptors with machine learning demonstrated peptide regulation of a wide range of target effector cells, including cells of muscular systems. The striking parallels between the peptidergic neuronal properties of Cnidaria and Bilateria and those of Ctenophora, the most basal neuron-bearing animals, suggest a common evolutionary origin of metazoan peptidergic nervous systems.

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Section: Discussionmentioning

confidence: 99%

Mass spectrometry of short peptides reveals common features of metazoan peptidergic neurons

et al. 2022

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“…The presence of a PNX peptide in choanoflagellates demonstrates that some animal neuropeptides have premetazoan origin and predate nervous systems. Many other neuronal molecules, including neurosecretory components ( Göhde et al 2021 ), postsynaptic proteins ( Burkhardt et al 2014 ), and voltage-gated channel subunits ( Moran and Zakon 2014 ), have a similar history, suggesting the stepwise assembly of the synaptic and neurosecretory machinery from pre-existing components at the origin of neurons ( Arendt 2020 ; Burkhardt and Jékely 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Neuropeptides play pivotal roles in the regulation of different biological processes such as feeding, cognition, and reproduction, and they have been extensively studied in bilaterians ( Jékely 2013 ; Mirabeau and Joly 2013 ; Elphick et al 2018 ; Thiel et al 2021 ). Neuropeptide-like molecules have also been described in cnidarians, ctenophores, and the neuron-less placozoan Trichoplax adhaerens ( Takahashi et al 2008 ; Jékely 2013 ; Senatore et al 2017 ; Varoqueaux et al 2018 ; Koch and Grimmelikhuijzen 2020 ; Takahashi 2020 ; Burkhardt and Jékely 2021 ; Sachkova et al 2021 ). So far, none of the neuropeptides described in these species has shown enough similarity to be considered direct orthologs of bilaterian short neuropeptides.…”

Section: Introductionmentioning

confidence: 99%

Premetazoan Origin of Neuropeptide Signaling

Yáñez-Guerra

Thiel

Jékely

2022

Molecular Biology and Evolution

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Neuropeptides are a diverse class of signalling molecules in metazoans. They occur in all animals with a nervous system and also in neuron-less placozoans. However, their origin has remained unclear because no neuropeptide shows deep homology across lineages and none have been found in sponges. Here, we identify two neuropeptide precursors, phoenixin and nesfatin, with broad evolutionary conservation. By database searches, sequence alignments and gene-structure comparisons we show that both precursors are present in bilaterians, cnidarians, ctenophores and sponges. We also found phoenixin and a secreted nesfatin precursor homolog in the choanoflagellate Salpingoeca rosetta. Phoenixin in particular, is highly conserved, including its cleavage sites, suggesting that prohormone processing occurs also in choanoflagellates. In addition, based on phyletic patterns and negative pharmacological assays we question the originally proposed GPR-173 (SREB3) as a phoenixin receptor. Our findings revealed that secreted neuropeptide homologs derived from longer precursors have pre-metazoan origins and thus evolved before neurons.

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“…The discovery of the non-synaptic architecture of the cydippid-phase SNN raises the intriguing question about the mechanism of signal propagation. Genome and single cell transcriptome analyses revealed that M. leidyi SNN neurons express several voltage gated calcium (Ca v ), 35 potassium (K v ) and two non-specific sodium (Na v ) channels 14,36,37 . These numbers are similar to neurons of other animals and ctenophore SNN neurons are therefore very likely to produce action potentials 38 .…”

Section: Discussionmentioning

confidence: 99%

Syncytial nerve net in a ctenophore sheds new light on the early evolution of nervous systems

Burkhardt

Medhus

Digel

et al. 2022

Preprint

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SummaryA fundamental breakthrough in neurobiology has been the formulation of the neuron doctrine by Santiago Ramón y Cajal, which states that the nervous system is composed of discrete individual cells. Electron microscopy later confirmed the doctrine and allowed the identification of synaptic connections. Here we use volume electron microscopy and 3D reconstructions to characterize the nerve net of a cydippid-phase ctenophore, belonging to one of the earliest-branching animal lineages. We found that neurons of its subepithelial nerve net do not follow Cajal’s neuron doctrine but instead show a continuous plasma membrane forming a syncytium. This is more similar to the reticulate theory of the nervous system put forward by Camillo Golgi. Additionally, we were able to identify new sensory cell types and describe simple neuro-sensory circuits for cydippid-phase ctenophores. Together with the ctenophore-specific synaptic architecture and the presence of an extensive repertoire of lineage-specific neuropeptides our morphological data provide substantial evidence for the independent evolution of the nervous system of ctenophores and the remaining animals.

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Evolution of synapses and neurotransmitter systems: The divide-and-conquer model for early neural cell-type evolution

Cited by 24 publications

References 101 publications

Mass spectrometry of short peptides reveals common features of metazoan peptidergic neurons

Mass spectrometry of short peptides reveals common features of metazoan peptidergic neurons

Premetazoan Origin of Neuropeptide Signaling

Syncytial nerve net in a ctenophore sheds new light on the early evolution of nervous systems

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