Glycans in adhesion and fertilization: histochemical and ultrastructural insights from the chaetognath Spadella...

To cope with the dynamic intertidal environment, some marine invertebrates have evolved carbohydrate-based adhesive mechanisms. Glycans are also involved in reproductive processes in protostomes, yet data about their distribution and function in chaetognaths are scarce. Among them, the benthic arrow worm Spadella cephaloptera can rapidly and temporarily attach to substrates, making it an interesting target for investigating the underlying glycobiology of its adhesion and reproductive systems. In this study, we characterized the distribution of different glycans in S. cephaloptera using histochemistry, immunofluorescence, lectin binding assays, and transmission electron microscopy, with a focus on the adhesive system during ontogeny.

Adhesive cells showed stage-specific distribution: in hatchlings, these cells form protrusions in the epidermis (papillae) and concentrate anteriorly, while in juveniles and adults, they group into multicellular adhesive cells forming clusters (compound papillae) in the posterior region. Ultrastructurally, the adhesive cells contain secretion granules enriched in fibrillar structures, and feature synaptic vesicles. Lectin binding revealed strong Peanut Agglutinin (PNA) affinity to the apical region of the cells, indicating the presence of Galβ1-3GalNAc moieties similar to other temporary adhesive systems. In addition, we detected acidic and sulfated mucosubstances in the sperm ducts, while a carboxylated jelly coat surrounds mature oocytes.

Our findings suggest that the ontogenetic shift of adhesive cells from the anterior to the posterior body region is correlated with the alimentary and foraging behavior during the life cycle of S. cephaloptera. Evidence from lectin-assays, histological stainings, and ultrastructural analyses reveals the involvement of glycans in both reproductive and adhesive systems, with patterns suggesting functional conservation of mechanisms present in other marine invertebrates. The observed glycan moieties in the adhesive cells of S. cephaloptera indicate convergently evolved traits, such as the presence of neutral mucosubstances and PNA-binding glycans, as reported for other temporary adhesive systems in marine invertebrates. This work provides a framework for a molecular characterization of the reproductive and adhesive systems of the enigmatic chaetognaths.