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

Abstract

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.

Alternative neural systems: What is a neuron? (Ctenophores, sponges and placozoans)

“…Each presynaptic region contains three layers of organelles: a layer of synaptic vesicles lining the presynaptic membrane, a cistern of agranular endoplasmic reticulum just above the row of vesicles, followed by one or several mitochondria. The non-polarized organization with the apparent ability to form synapses everywhere and symmetrical synapses was also demonstrated (Hernandez-Nicaise, 1973c;Hernandez-Nicaise, 1991) and confirmed by recent reconstruction (Sachkova et al, 2021;Burkhardt et al, 2022).…”

“…We can now distinguish more than 20 morphologically different populations of neurons and five types of receptors in each studied species (Norekian and Moroz, 2019a;2020). Surprisingly, at least five neurons in the early post-hatching stages of Mnemiopsis can form a syncitium with fused plasma membranes (Sachkova et al, 2021;Burkhardt et al, 2022). Such syncytial-type of networks are relatively rare in nature.…”

Evolution of the ribbon-like organization of the Golgi apparatus in animal cells

“…We then analyzed cnidarians: in the hydrozoan Clytia hemisphaerica , the secretory gland cells of the gastroderm, but not other cell types, display stacks linked into a ribbon-like structure (Figure 2E), which is also observed in phagocytic cells of another cnidarian, the actinia Phelliactis robusta 40 . In the ctenophore Mnemiopsis leidyi , epithelial and comb cells (Figure 2F and S2E), nerve net neurons, mesogleal neurons, and sensory cells 41,42 all display separated stacks. Among other animals, we found a single Golgi stack in all cells of two placozoan species: Trichoplax adhaerens (Figure 2G, S2C and S2D) and Hoilungia hongkongensis 43 .…”

“…Strongylocentrotus purpuratus, Platynereis dumerilii , Mnemiopsis leidyi , Oscarella carmela and Capsaspora owczarzaki samples were high-pressure frozen, freeze substituted and processed as described S7,10–14 .…”

The premetazoan ancestry of the synaptic toolkit and appearance of first neurons

“…As discussed in the second section, as more detailed information about the molecular components and structure of neurons and synapses in non-bilaterians comes out, the question of a single or multiple origins becomes less clear. Ctenophores possess unique synaptic structures (so-called pre-synaptic triads) and anastomosed neurites in their nerve net, unlike anything reported in other nervous systems [ 124 , 202 ]. Likewise, cnidarians have an incompletely understood synaptic toolkit, many bidirectional synapses, and multifunctional neurons.…”