Divergent dynamics in whole-body regeneration and larval development of sponge Haliclona simulans: cytobiology, microbiome, and transcriptomics.

Sponges are capable of rebuilding functional individuals from cell aggregates (primmorphs), a process termed whole-body regeneration that morphologically parallels larval development. To systematically compare these processes, we established an in vitro primmorph regeneration model in Haliclona simulans and performed multi-level analyses across planktonic, settled, and metamorphic stages. Although both processes formed similar structures (e.g., the aquiferous system), planktonic primmorphs exhibited a reduced stem cell proportion (archeocyte/choanocyte), along with the increase of seemingly dedifferentiating cells and vacuolar cells. Microbiome diverged: while sharing core symbionts (e.g., AqS1), primmorphs enriched Tenacibaculum and Vibrio species during remodeling process. Transcriptomics revealed distinct signatures: regeneration upregulated genes potentially related to DNA repair and dedifferentiation but downregulated stem cell markers. Our integrative study indicates that regeneration and development constitute distinct processes, achieving similar functional outcomes via divergent cellular, microbial, and molecular profiles that provides a foundational framework for future mechanistic studies of regeneration.