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. Porifera seem to be one of the best candidates to be the sister group to all other Metazoa. This makes them a key taxon to explore cell-adhesion evolution on animals. For this reason, several transcriptomic, genomic, histological, physiological and biochemical studies focused on sponge epithelia. Nevertheless, the complete and precise protein composition of cell–cell junctions and mechanisms that regulate epithelial morphogenetic processes still remain at the center of attention. 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 adhaerens-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 a non-bilaterian lineage by combining fluorescent and electron 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.

Tissue homeostasis in sponges: Quantitative analysis of cell proliferation and apoptosis

“…Sponge cells do, however, form discrete functional units that can be called tissues, for example, choanoderm, exo-, and endopinacoderm (Leys & Hill, 2012;Leys et al, 2009). In most species, these tissues lack conventional epithelial features like well-developed intracellular junctions or basal membrane, yet they are able to function as true epithelia, occluding the internal milieu of the animal (Adams et al, 2010) and taking part in epithelial morphogenesis Vernale et al, 2021). Here we show that sponge tissues (especially epithelial-like choanoderm) also maintain homeostasis through constant cell turnover, as it occurs in "higher" animals.…”

First draft genome assembly and characterization of spongeHalisarca dujardiniireveals key components of basement membrane and broad repertoire of aggregation factors

“…Type IV collagen was previously discovered among sponges by BLAST and phylogenetic analysis in Corticium candelabrum (Homoscleromorpha) and Sycon coactum (Calcarea) (Leys and Riesgo, 2012). Experimental confirmation of the localization of this protein in the basal membrane was obtained in homoscreromorphs Pseudocorticium jarrei and O. lobularis 3,5 . We searched the proteome of H. dujardinii for homologs of collagen IV, fibrillar collagens, and spongins.…”

“…The class Demospongiae, or common sponges, is the largest, and includes sponges with a skeleton made of silicon oxide or organic substance (spongin) 2 . The class Homoscleromorpha has recently been separated from the class Demospongiae, and includes sponges with the most advanced features of Eumetazoa: basement membrane contained collagen type IV and adherens-like intercellular junctions [3][4][5] .…”

A broad‐taxa approach as an important concept in ecotoxicological studies and pollution monitoring

“…The cells within the primmorph then differentiate and small fragments that attach to the substrate form new sponges by extending their structures (Lavrov & Kosevich, 2014, 2016; Ereskovsky et al ., 2021). Differentially expressed genes, and some of the mechanisms underlying the dissociation–reaggregation phenomena in the sponge Oscarella lobularis have been revealed (Vernale et al ., 2021). Heavy metals influence the behaviour of cells in the reaggregation process (Cebrian & Uriz, 2007 b , c ).…”