Independent Innexin Radiation Shaped Signaling in Ctenophores

Abstract

Innexins facilitate cell-cell communication by forming gap junctions or non-junctional hemichannels, which play important roles in metabolic, chemical, ionic, and electrical coupling. The lack of knowledge regarding the evolution and role of these channels in ctenophores (comb jellies), the likely sister group to the rest of animals, represents a substantial gap in our understanding of the evolution of intercellular communication in animals. Here we identify and phylogenetically characterize the complete set of innexins of four ctenophores: Mnemiopsis leidyi, Hormiphora californensis, Pleurobrachia bachei, and Beroe ovata. Our phylogenetic analyses suggest that ctenophore innexins diversified independently from those of other animals and were established early in the emergence of ctenophores. We identified a four-innexin genomic cluster, which was present in the last common ancestor of these four species and has been largely maintained in these lineages. Evidence from correlated spatial and temporal gene expression of the M. leidyi innexin cluster suggest that this cluster has been maintained due to constraints related to gene regulation. We describe basic electrophysiological properties of putative ctenophore hemichannels from muscle cells using intracellular recording techniques, showing substantial overlap with the properties of bilaterian innexin channels. Together, our results suggest that the last common ancestor of animals had gap junctional channels also capable of forming functional innexin hemichannels, and that innexin genes have independently evolved in major lineages throughout Metazoa.

Syncytial nerve net in a ctenophore adds insights on the evolution of nervous systems

“…Whereas gap junctions could be identified within the comb plates, as previously reported ( 15 ) in our SBFSEM data as well as in TEM micrographs, we found no evidence of similar structures between neurites of nerve-net neurons that would suggest the presence of electrical synapses. Additionally, a recent characterization of the complete set of M. leidyi innexins—responsible for the formation of gap junctions in invertebrates—did not show any mRNA expression in in situ hybridization experiments in nerve-net cell bodies ( 23 ). However, we did observe synaptic triads and plasma membrane contacts of unknown molecular structure that connect the SNN externally to polster and mesogleal neurons.…”

Evolutionary origin of the nervous system from Ctenophora prospective

“…As a wider range of modern techniques has recently become available in ctenophores (e.g., single‐cell RNAseq [Sebé‐Pedrós et al, 2018] and connectomics [Burkhardt et al, 2023]) and ctenophore species have progressed towards becoming established lab models (e.g., culturing and CRISPR/Cas9 knock‐outs have been reported [Presnell et al, 2022; Soto‐Àngel et al, 2022]), new critical insights into the biology of their neurons have been revealed. Earlier studies have established such key approaches as electrophysiology and calcium imaging in ctenophores; however, it has been achieved only in comb plates (Moss & Tamm, 1987; Tamm & Terasaki, 1994) and muscles (Moroz et al, 2014; Ortiz et al, 2023), while direct measurements of neuronal activity have not been reported. Thus, more experimental approaches are urgently required to understand the function of ctenophore neurons.…”

Morphological and dietary changes encoded in the genome of Beroe ovata, a ctenophore-eating ctenophore

“…We performed differential gene expression analyses on the B. ovata transcriptomic data we generated and on previously published transcriptomic data collected from the comb rows ( 35 ) and the aboral organs ( 76 ) of adult M. leidyi . These comparisons were used to investigate tissue-defining genes shared by the last common ancestor of B. ovata and M. leidyi .…”