Insights into the evolutionary origins of neurons from functions of putative neurogenic transcription factors in Ctenophora
by Minato Miyake | Osamu Horiguchi | Hiroshi Watanabe | Okinawa Institute of Science and Technology (OIST) | Okinawa Institute of Science and Technology (OIST) | Okinawa Institute of Science and Technology (OIST)
Abstract ID: 38
Event: The 3rd AsiaEvo Conference
Topic: Marine evo-devo: new frontiers from emerging marine model organisms
Presenter Name: Minato Miyake

The arise of the nervous system is a hallmark of animal evolution, yet little is known of the evolutionary origins and characteristics of neurons in ancestral animals. To answer this, Ctenophora are an optimal target of investigation, as they are the earliest-branching extant animal lineage with neurons. However, ctenophores do not seem to possess major neural genes and neurotransmitters known in Cnidaria/Bilateria (1). A recent study also revealed ctenophores to develop a syncytial neural network of subepithelial neurons (2). These data indicate that the ctenophore nervous system consists of, at least in part, unique molecular and structural features which may have evolved independently from other metazoans. Nonetheless, the molecular mechanisms responsible for their neurogenesis remain unclear, making it difficult to reconstruct the initial processes of neuronal evolution.

Recently, our lab identified multiple neuropeptides of the new model ctenophore Bolinopsis mikado, revealing common genetic features of neurosecretory machinery between ctenophore and cnidarian/bilaterian peptidergic neurons (3). By using these neuropeptides as definitive neural markers of Ctenophora, we found that transcription factors (TFs), such as bHLH, POU, and SOX, which are pivotal for neurogenesis in Cnidaria/Bilateria, are expressed in neural cell clusters of the ctenophore single-cell RNA-seq dataset. Here, we present our recent progress on expressional and functional analyses of these potential neurogenic TFs in B. mikado larvae. In particular, morpholino oligo knock-down of target TFs was performed, and downstream genes were investigated using RNA-seq. Ultimately, the results are hoped to help elucidate the extent to which neurogenic mechanisms are conserved across all animal lineages and provide insights to reconstruct the initial processes of neuronal evolution.

(1) Moroz, L. L., Kocot, K. M., Citarella, M. R. et al. (2014). The ctenophore genome and the evolutionary origins of neural systems. Nature510(7503), 109–114.
(2) Burkhardt, P., Colgren, J., Medhus, A. et al. (2023). Syncytial nerve net in a ctenophore adds insights on the evolution of nervous systems. Science., 380(6642), 293–297.
(3) Hayakawa, E., Guzman, C., Horiguchi, O. et al. (2022). Mass spectrometry of short peptides reveals common features of metazoan peptidergic neurons. Nature ecology & evolution6(10), 1438–1448.