Evidence for an Alternative Mechanism of Toxin Production in the Box Jellyfish Alatina alata.

Abstract

Cubozoans (box jellyfish) have a reputation as the most venomous animals on the planet. Herein, we provide a review of cubozoan prey capture and digestion informed by the scientific literature. Like all cnidarians, box jellyfish envenomation originates from structures secreted within nematocyte post-Golgi vesicles called nematocysts. When tentacles come in contact with prey or would-be predators, a cocktail of toxins is rapidly deployed from nematocysts via a long spiny tubule that serves to immobilize the target organism. The implication has long been that toxin peptides and proteins making up the venom within the nematocyst capsule are secreted directly by nematocytes during nematogenesis. However, our combined molecular and morphological analysis of the venomous box jellyfish Alatina alata suggests that gland cells with possible dual roles in secreting toxins and toxic-like enzymes are found in the gastric cirri. These putative gland cell assemblages might be functionally important internally (digestion of prey) as well as externally (envenomation) in cubozoans. Despite the absence of nematocysts in the gastric cirri of mature A. alata medusae, this area of the digestive system appears to be the region of the body where venom-implicated gene products are found in highest abundance, challenging the idea that in cnidarians venom is synthesized exclusively in, or nearby, nematocysts. In an effort to uncover evidence for a central area enriched in gland cells associated with the gastric cirri we provide a comparative description of the morphology of the digestive structures of A. alata and Carybdea box jellyfish species. Finally, we conduct a multi-faceted analysis of the gene ontology terms associated with venom-implicated genes expressed in the tentacle/pedalium and gastric cirri, with a particular emphasis on zinc metalloprotease homologs and genes encoding other bioactive proteins that are abundant in the A. alata transcriptome.