Evolution of mechanisms controlling epithelial morphogenesis across animals: new insights from dissociation - reaggregation experiments in the sponge Oscarella lobularis

Abstract

Background: The ancestral presence of epithelia in Metazoa is no longer debated. Even though Porifera seem to be the best candidates to be the sister group to all other Metazoa, hardly anything is known about the proteins involved in the composition of cell-cell junctions or about the mechanisms that regulate epithelial morphogenetic processes in this phylum. Results: To get insights into the early evolution of epithelial morphogenesis, we focused on morphogenic characteristics of the homoscleromorph sponge Oscarella lobularis. Homoscleromorpha are a sponge class with a typical basement membrane and adherens-like junctions unknown in other sponge classes. We took advantage of the dynamic context provided by cell dissociation-reaggregation experiments to explore morphogenetic processes in epithelial cells in an early lineage by combining fluorescent and electronic microscopy observations and RNA sequencing approaches at key time-points of the dissociation and reaggregation processes. Conclusions: Our results show that part of the molecular toolkit involved in the loss and restoration of epithelial features such as cell-cell and cell-matrix adhesion is conserved between Homoscleromorpha and Bilateria, suggesting their common role in the last common ancestor of animals. In addition, Sponge-specific genes are differently expressed during the dissociation and reaggregation processes, calling for future functional characterization of these genes.

The sponge Oscarella lobularis (Porifera, Homoscleromorpha) as a suitable biomonitor of metallic contamination in Mediterranean coastal ecosystems

“…The present results ar''also expected to be useful for future ecotoxicological studies. Indeed, Oscarella lobularis is now one of the best described Mediterranean sponge species at chemical, physiological, morphological, reproductive, cellular and molecular levels (Belahbib et al, 2018;Ereskovsky et al, 2015;Fierro-Constain et al, 2017;Renard et al, 2021;Rocher et al, 2020;Vernale et al, 2021), thereby enabling integrative approaches. samples and providing efficient lab facilities.…”

“…In this context, Oscarella lobularis (Schmidt, 1862) provides several advantages: i) being abundant in shallow rocky substrates of the north-western Mediterranean Sea, including at the vicinity of the Marseille Metropole and the French Riviera (Ereskovsky et al, 2009;Renard et al, 2021). Oscarella lobularis is part of the coralligenous biocenosis which represents a biodiversity hotspot in Mediterranean ecosystems (Bertolino et al, 2013;Martin et al, 2014); ii) the taxonomic identification of the species is clear (Gazave et al, 2012(Gazave et al, , 2013 and the life cycle, development and morphoanatomical organization were deeply studied (Ereskovsky et al, 2009Fierro-Constain et al, 2017); iii) the high regeneration capability (Ereskovsky et al, 2015) and the high number of buds obtained in vitro by asexual reproduction Rocher et al, 2020) provide useful replicates for experimental ecotoxicological studies; iv) in addition, both genomic and transcriptomic resources (Belahbib et al, 2018;Schenkelaars et al, 2015;Vernale et al, 2021) and molecular tools are available for this species (Borchiellini et al, 2021;Fierro-Constain et al, 2017;Fierro-Constaín et al, 2021;Renard et al, 2021;Rocher et al, 2020). This is convenient and suitable to perform ecotoxicological experiments at different complementary levels of the biological scale (from morphological, to physiological, cellular, and molecular levels).…”