Genomes of Solenogastres Shed Light on Ancestral Molluscan Biomineralization Genes

Aplacophora (Solenogastres + Caudofoveata) is a group of worm-like molluscs that lack a shell and instead are covered with aragonitic spines and scales called sclerites. Sclerites are also found along the girdle in chitons (Polyplacophora) and are a synapomorphy for Aculifera (Aplacophora + Polyplacophora), which is the sister taxon of all other shell-bearing molluscs (Conchifera). However, whether the same genetic mechanism underlies the process of biomineralization in aculiferans and conchiferans is unknown. To investigate evolution of genes involved in biomineralization across Mollusca, we re-sequenced the genomes of two species of Solenogastres, Epimenia babai and Neomenia megatrapezata , producing near-chromosome-level assemblies through PacBio HiFi and Hi-C scaffolding. Using a combination of orthology inference and similarity searches against a known SMP database we identified 1,244 putative SMP orthogroups across Mollusca, 292 of which were present in at least one solenogaster genome. SMPs undergoing significant expansion/contraction at key nodes were further investigated. Of these, 15 were found in at least one solenogaster genome and included families containing chitin-binding, von Willebrand factor A, and C-type lectin domains. Across Mollusca, Solenogastres showed the highest number of significant losses in all gene families, including the SMPs investigated. Targeted searches for structural, silk-like proteins in Aculifera show further reductions in Solenogastres (16-17) compared to caudofoveates (29) and chitons (46-80). Altogether, our results support a conserved but reduced biomineralization toolkit underlying sclerite formation in Solenogastres and identify candidate genes for further proteomic and functional study.