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

Abstract

BackgroundTo cope with strong and rapidly changing water currents, some marine invertebrates have evolved complex adhesive mechanisms that involve the interplay of different biomolecules, such as carbohydrates. Carbohydrates may, however, also be involved in other physiological processes such as reproduction, a research field poorly studied in protostomes. The benthic chaetognath Spadella cephaloptera is a protandric hermaphrodite capable of rapid attachment and detachment to substrates. Nevertheless, the putative underlying glycobiology during the adhesion process but also other physiological processes remain unknown for chaetognaths. MethodsIn the present study, through histological, immunohistochemical, and ultrastructural analysis, we characterized the location of different glycans in the reproductive and attachment systems of S. cephaloptera. Developmental changes of adhesive cells were investigated from early hatchlings up to adults. ResultsAcidic and sulfated mucosubstances were detected in the sperm ducts, whereas mature oocytes were surrounded by a carboxylated jelly coat. The distribution of adhesive cells in S. cephaloptera shifted from anterior discrete individual cells in hatchlings to posteriorly distributed cell clusters in the adult. Moreover, we identified secretion granules enriched in fibrous content inside the adhesive cells. Furthermore, immunohistochemistry revealed microtubule processes linking the adhesive cells to the intraepidermal plexus. Lectin affinity tests showed strong apical PNA binding and clear PHA-L/E and ConA signals in the adhesive cells. No evidence for a dual gland detachment system was observed. ConclusionsThis study provides the first glycan distribution analysis in a chaetognath, revealing the presence of carbohydrates in different structures of the reproductive system, highlighting their putative relevance during the fertilization process. Furthermore, the observed glycan moieties suggest that S. cephaloptera also combines convergently evolved features reported for other temporary attachment systems in marine invertebrates. However, S. cephaloptera also displays unique characters, such as specific ontogenetic changes occurring during early developmental stages that correspond to its feeding behavior. Our observations do not support the presence of additional gland cells mediating detachment. Finally, this work sets the framework for a molecular characterization of the reproductive and attachment systems of the enigmatic chaetognaths.