Regeneration in spongeSycon ciliatummimics postlarval development

Abstract

Somatic cells dissociated from an adult sponge can re-organize and develop into a functional juvenile. However, the extent to which regeneration recapitulates embryonic developmental signaling pathways has remained enigmatic for more than a century. To this end, we have standardized and established a sponge Sycon ciliatum regeneration protocol to achieve consistent regeneration in cell culture. From the morphological analysis, we demonstrated that dissociated sponge cells follow a series of morphological events resembling embryonic and postlarval development. Hence, we propose that sponge regeneration represents somatic development. To support our hypothesis, we performed high-throughput sequencing on regenerating samples and compared the data with regular embryonic and postlarval development of Sycon ciliatum. Our comparative transcriptomic analysis illuminates that sponge regeneration is equally as dynamic as embryogenesis. We find that sponge regeneration is orchestrated by complex regulatory mechanisms by recruiting signaling pathways like those utilized in embryonic development to organize into a functional juvenile. In the current study, we lay down the basic framework to study Sycon ciliatum regeneration. Since sponges are likely to be the first branch of extant multicellular animal and the sister lineage to nearly all animals, we suggest that this system can be explored to study the genetic features underlying the evolution of multicellularity and regeneration.

Fast transcriptional activation of developmental signalling pathways during wound healing of the calcareous sponge Sycon ciliatum

“…On the other hand, programmed cell death has been increasingly identified as a key prerequisite for successful wound healing and regeneration in animals in the past decade [39,40,79,80,81,82,83]. Only very recent studies have investigated the role of apoptosis in sponge regeneration, revealing its involvement in re-development from dissociated cells in S. ciliatum [28]. The importance of apoptosis for tissue remodelling remains obscure, as although two waves of apoptosis during demosponge Aplysina cavernicola regeneration were detected using the TUNEL assay method, no evidence for an increase of apoptosis-related genes could be found during Halisarca caerulea regeneration [22,86].…”

“…Syconoid sponges in particular represent unique candidates for comparative regenerative studies, given their radial symmetry around a directional, apical to basal, axis and extensive developmental regulatory gene toolkit [25,26,27,28]. Although sponges from the genus Sycon have long been known for their remarkable regeneration abilities, only recent research has provided transcriptomic insight into restoration from dissociated cells including comparison to postembryonic development in S. ciliatum [29], a calcareous sponge found along the coasts of Atlantic Europe [28,30,31]. However, S. ciliatum whole body or structural regeneration has not been previously studied using genomic and modern microscopic tools.…”

“…While calcareous sponges have been subject of extensive developmental studies over the last century and have provided valuable insights into early animal evolution, only few studies on regeneration in Calcarea are available -mostly restricted to morphological and histological observations [12]. Syconoid sponges in particular represent unique candidates for comparative regenerative studies, given their radial symmetry around a directional, apical to basal, axis and extensive developmental regulatory gene toolkit [25,26,27,28]. Although sponges from the genus Sycon have long been known for their remarkable regeneration abilities, only recent research has provided transcriptomic insight into restoration from dissociated cells including comparison to postembryonic development in S. ciliatum [29], a calcareous sponge found along the coasts of Atlantic Europe [28,30,31].…”

The salamander blastema within the broader context of metazoan regeneration

“…Indeed, when we look at the most basal metazoans, we see that the lines between these processes are somewhat blurred (Bely and Nyberg, 2010;Gold and Jacobs, 2013). Many sponges and cnidarians redeploy developmental processes throughout their lifecycle: symmetry breaking and patterning are redeployed in the adult to enforce the appropriate spacing of repeating structures during growth and reproduction (Lengfeld et al, 2009;Watanabe et al, 2014;Soubigou et al, 2020). In particular, Wnt signaling, FGF signaling, and BMP/ TGF-β signaling are all employed during regeneration and development in sponges and cnidarians (Gold and Jacobs, 2013;Maddaluno et al, 2017;Slack, 2017;Soubigou et al, 2020;Tursch and Holstein, 2023), and all have significant roles in the axolotl blastema (McCusker et al, 2015;Vincent et al, 2020).…”

The Hazards of Regeneration: From Morgan’s Legacy to Evo-Devo

“…This holds true for their regenerative mechanisms that show great inter-species variations. For instance, the proverbial ability of cell aggregates to generate a functional sponge varies even between closely related species [51][52][53][54]: Halisarca dujardini can reconstruct its body from cell suspension, whereas Halisarca panicea is unable to do so [53]. Whether or not cell reaggregation is ancestral to Porifera will remain unsolved without phylum-level comparative studies.…”