A new transcriptome and transcriptome profiling of adult and larval tissue in the box jellyfish Alatina alata: an emerging model for studying venom, vision and sex.

BACKGROUND: Cubozoans (box jellyfish) are cnidarians that have evolved a number of distinguishing features. Many cubozoans have a particularly potent sting, effected by stinging structures called nematocysts; cubozoans have well-developed light sensation, possessing both image-forming lens eyes and light-sensitive eye spots; and some cubozoans have complex mating behaviors, including aggregations, copulation and internal fertilization. The cubozoan Alatina alata is emerging as a cnidarian model because it forms predictable monthly nearshore breeding aggregations in tropical to subtropical waters worldwide, making both adult and larval material reliably accessible. To develop resources for A. alata, this study generated a functionally annotated transcriptome of adult and larval tissue, applying preliminary differential expression analyses to identify candidate genes involved in nematogenesis and venom production, vision and extraocular sensory perception, and sexual reproduction, which for brevity we refer to as "venom", "vision" and "sex". RESULTS: We assembled a transcriptome de novo from RNA-Seq data pooled from multiple body parts (gastric cirri, ovaries, tentacle (with pedalium base) and rhopalium) of an adult female A. alata medusa and larval planulae. Our transcriptome comprises ~32 K transcripts, after filtering, and provides a basis for analyzing patterns of gene expression in adult and larval box jellyfish tissues. Furthermore, we annotated a large set of candidate genes putatively involved in venom, vision and sex, providing an initial molecular characterization of these complex features in cubozoans. Expression profiles and gene tree reconstruction provided a number of preliminary insights into the putative sites of nematogenesis and venom production, regions of phototransduction activity and fertilization dynamics in A. alata. CONCLUSIONS: Our Alatina alata transcriptome significantly adds to the genomic resources for this emerging cubozoan model. This study provides the first annotated transcriptome from multiple tissues of a cubozoan focusing on both the adult and larvae. Our approach of using multiple body parts and life stages to generate this transcriptome effectively identified a broad range of candidate genes for the further study of coordinated processes associated with venom, vision and sex. This new genomic resource and the candidate gene dataset are valuable for further investigating the evolution of distinctive features of cubozoans, and of cnidarians more broadly.

Raising Awareness of the Severity of "Contactless Stings" by Cassiopea Jellyfish and Kin.

Discussion around avoidance and mitigation of jellyfish stings has traditionally focused on swimmers and divers being mindful of their behavior relative to swimming medusae (pelagic jellyfish). This framework must be restructured with the inclusion of the oblique risk posed by novel autonomous stinging structures like cassiosomes from Cassiopea (a jellyfish genus of the taxonomic order Rhizostomeae). Cassiosomes are released by Cassiopea sp. into subtropical waters that can consequently sting human skin, causing varying degrees of pain and irritation; this trait extends to other rhizostome jellyfish species. Swimmers and waders may put themselves at risk simply by coming into contact with agitated water in the vicinity of Cassiopea medusae, even without touching any part of the jellyfish (medusa, tentacles, or otherwise). Herein, we highlight details provided by 46 researchers and professional aquarists reporting incidents in which they experienced "stinging water" sensations, which we also refer to as "contactless stings''. We report these findings in order to increase the awareness of a public safety hazard the community may be unaware of in their own labs, aquariums, and sampling locations.

Medusa: A Review of an Ancient Cnidarian Body Form.

Medusae (aka jellyfish) have multiphasic life cycles and a propensity to adapt to, and proliferate in, a plethora of aquatic habitats, connecting them to a number of ecological and societal issues. Now, in the midst of the genomics era, affordable next-generation sequencing (NGS) platforms coupled with publically available bioinformatics tools present the much-anticipated opportunity to explore medusa taxa as potential model systems. Genome-wide studies of medusae would provide a remarkable opportunity to address long-standing questions related to the biology, physiology, and nervous system of some of the earliest pelagic animals. Furthermore, medusae have become key targets in the exploration of marine natural products, in the development of marine biomarkers, and for their application to the biomedical and robotics fields. Presented here is a synopsis of the current state of medusa research, highlighting insights provided by multi-omics studies, as well as existing knowledge gaps, calling upon the scientific community to adopt a number of medusa taxa as model systems in forthcoming research endeavors.

Gonadal histology of box jellyfish (Cnidaria: Cubozoa) reveals variation between internal fertilizing species Alatina alata (Alatinidae) and Copula sivickisi (Tripedaliidae).

Cubozoans (box jellyfish) are gonochoristic cnidarians with distinct reproductive strategies. This comparative histological study examines the gonad organization of Alatina alata and Copula sivickisi, two box jellyfish species that exhibit different modes of internal fertilization. A. alata reproduces via spermcasting aggregations while C. sivickisi reproduces via copulation; in both cases, internal fertilization occurs in the gastrovascular cavity. Herein, we provide the first histological description of subgastric sacs-structures unique to C. sivickisi. Although previously thought to function as sperm storage sacs, our findings reveal that subgastric sacs are nematocyst nests lacking sperm entirely. Conversely, we discovered that velarial spots in C. sivickisi females correspond to actual sperm storage structures. Histological examination of cubozoan sperm packages revealed that while sperm packages from both species have motile flagella, A. alata males produce nonencapsulated sperm bundles (i.e., "spermatozeugmata"), and C. sivickisi males produce encapsulated packages (i.e., "spermatophores"). Our findings corroborate the presence of several types of nematocysts in C. sivickisi embryo strands and spermatophores, and indicate their provenance to be both female and male gonads respectively, as well as subgastric sacs (i.e., nematocyst nests). In contrast to our findings of velarial spots as sperm storages structures in C. sivickisi females, and of nematocysts in the gonads of both sexes, we report that A. alata medusae lack both sperm storage structures and gonadal nematocysts. Finally, we discuss our findings on reproductive morphology of C. sivickisi and A. alata in light of the respective reproductive behavior of these two cubozoan species.

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

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.