Search bioRxiv⌕ Search

Biology subjects

Ferraioli, A.

Publications and source records attributed to Ferraioli, A..

6 recordsLinked to original sources

Ancient nervous system architecture in a living ctenophore

The evolutionary origin of nervous systems in animals remains elusive and is largely hidden from the fossil record. Ctenophores, one of the earliest-branching animals possessing neurons, are instrumental to our understanding of nervous system origin, and a few rare ctenophore fossils preserve traces of nervous tissue as carbonaceous remains. Cambrian ctenophores appear to exhibit a more diverse neuroanatomy than that of modern species, suggesting secondary loss in extant ctenophores. However, much remains unknown about the origin and ontogeny giving rise to the structural organization of modern ctenophore nervous systems. Here, by investigating the neural anatomy of the ctenophore Mnemiopsis leidyi during development, we identified a ladder-like nerve net (LNN) beneath the comb rows that converges into condensed neurites and connects to the aboral organ. Examination of carbon-rich areas of Ctenorhabdotus capulus, an extinct ctenophore from the Burgess Shale, reveals a pattern similar to that of M. leidyi, consistent with a shared neural organization. Furthermore, M. leidyi exhibits a condensed comb nerve, resembling the longitudinal nerve preserved in the Cambrian ctenophore Fasciculus vesanus and the giant axon of extant Euplokamis dunlapae. Our study reveals conserved evolutionary constraints shaping nervous system architectures linked to locomotory organs and indicates that the different modes of nervous system organization observed in Cambrian ctenophores are variably retained in modern species.

neuroscience↗

Life-stage-specific specialities in the cell atlases of the Clytia hemisphaerica planula and medusa

Jellyfish have complex life-cycles, but there has been limited exploration of how this is achieved at the cellular level. We used single-cell transcriptomics to assemble a cell atlas for the planula larva of Clytia hemisphaerica, and compared it to an updated cell atlas for the medusa (jellyfish) stage. The cells of the planula fell into the same broad categories as for the medusa: ectoderm, gastroderm, interstitial cells (i-cells), nematocytes (stinging cells), neurons and secretory cells. Although the planula cells generally showed less diversity than medusae within each category, cells with specialized features unique to their stage could be distinguished by their transcriptional profiles as well as by ultrastructure. Some planula-specific types were identified: aboral secretory cells involved in settlement, and a cell type attributed a role in immunity or post-metamorphic theca production. Distinct transcriptome profiles within different regions of the ciliated planula ectoderm reflected different post-metamorphosis fates of domains along the oral-aboral axis. Inspection of the cell clusters showing significant similarity of marker genes between planula and medusa, and inference of similarity using a statistical model of marker gene presence/absence, revealed correspondences between families of cells from planula and medusa rather than precise cell identities.

evolutionary biology↗

Dual origins for neural cells during development of the Clytia planula larva

Adult hydrozoan cnidarians undergo extensive tissue turnover, generating neural cell types including nematocytes (stinging cells) and gland cells from interstitial stem cells (i-cells) expressing stemness proteins such as Piwi and Nanos. The contribution of i-cells during embryogenesis, however, has been unclear. Here we address the origin of neural cells during development of the Clytia hemisphaerica planula larva. Marker gene in situ hybridisation revealed that Piwi/Nanos1-expressing cells within the early gastrula presumptive endoderm generate a substantial pool of nematoblasts, a few of which migrate and differentiate in the planula ectoderm. Some neurogenic and neuronal markers, however, showed a markedly distinct expression profile, developing within a basal layer of the aboral/lateral ectoderm during gastrulation. Embryo bisection and lineage tracing experiments confirmed that sensory neurons and secretory cell types derive from gastrula ectoderm, while nematocytes and at least some ganglionic neurons derive from i-cells. Knockdown and inhibitor treatments revealed steps in neuron and nematocyte development regulated by Wnt-{beta}-catenin. We conclude that two distinct neurogenesis pathways operate during Clytia embryogenesis, one involving aboral ectoderm delamination, and one generating mainly nematocytes from i-cell-like precursors. Summary statementDuring embryogenesis in the hydrozoan Clytia neural cell types derive both from Piwi/Nanos expressing "i-cells" and from ectodermal delamination during gastrulation.

developmental biology↗

The 3D architecture of the ctenophore aboral organ and the evolution of complex integrative centers in animals

The ability to sense and respond to environmental cues is fundamental to animal behavior and survival. In ctenophores - early-branching marine animals - a syncytial nerve net underlies complex behaviors such as geotaxis, feeding, and escape. At the center of this system is the aboral organ (AO), a dense sensory hub that detects motion, light, and pressure and coordinates ciliary movement. However, the AOs cellular architecture and its integration with the nerve net remain poorly understood. Here, using volume electron microscopy in Mnemiopsis leidyi, we reveal that the syncytial nerve net converges and condenses around the AO, forming synaptic connections with diverse effector cells. We annotated 17 distinct cell types, including candidate light and pressure sensors, novel ciliated and secretory cells, and non-synaptic vesicle-rich cells likely involved in volume transmission. Our data shows that signal processing within the AO relies on both synaptic and non-synaptic communication. Gene expression profiling of conserved transcription factors indicates that the AO is a functionally convergent, evolutionarily distinct sensory structure that retains minimal homology. Our findings redefine the ctenophore AO as a highly integrated, multilayered sensory system critical for behavioral regulation.

evolutionary biology↗

Aboral cell types of Clytia and coral larvae have shared features and link taurine to the regulation of settlement

Planktonic larvae of many marine invertebrates settle on a suitable substrate and metamorphose into bottom-dwelling adults. Larval settlement is of considerable interest both for ecologists and for evolutionary biologists, who have proposed that anterior sensory systems for substrate selection provided the basis for animal brains. Nevertheless the cellular and molecular regulation of larval settlement, including in Cnidaria (corals, jellyfish, sea anemones, hydroids) is not well understood. We generated and compared anterior (aboral) transcriptomes and single-cell RNA-seq datasets from the planula larvae of three cnidarian species: the hydrozoan jellyfish Clytia hemisphaerica, and the scleractinian corals Astroides calycularis and Pocillopora acuta. Integrating these datasets and characterizing aboral cell types, we defined a common cellular architecture of the planula aboral end, and identified clade-specific specializations in cell types, including unique aboral neural cells in the Clytia planula and neurosecretory cell types with distinct molecular signatures in both Clytia and coral planulae. Among common planula aboral features were genes implicated in taurine uptake and catabolism expressed in distinct specialized cell types. In functional assays, exogenous taurine inhibited settlement of both Clytia and Astroides planulae. These findings define a detailed molecular and cellular framework of the planula aboral pole, and implicate localized taurine destruction in defining settlement competence.

evolutionary biology↗

Whole Animal Multiplexed Single-Cell RNA-Seq Reveals Plasticity of Clytia Medusa Cell Types

We present an organism-wide, transcriptomic cell atlas of the hydrozoan medusa Clytia hemisphaerica, and determine how its component cell types respond to starvation. Utilizing multiplexed scRNA-seq, in which individual animals were indexed and pooled from control and perturbation conditions into a single sequencing run, we avoid artifacts from batch effects and are able to discern shifts in cell state in response to organismal perturbations. This work serves as a foundation for future studies of development, function, and plasticity in a genetically tractable jellyfish species. Moreover, we introduce a powerful workflow for high-resolution, whole animal, multiplexed single-cell genomics (WHAM-seq) that is readily adaptable to other traditional or non-traditional model organisms.

systems biology↗