The Dynamically Evolving Nematocyst Content of an Anthozoan, a Scyphozoan, and a Hydrozoan

Abstract

Nematocytes, the stinging cells of cnidarians, are the most evolutionarily ancient venom apparatus. These nanosyringe-like weaponry systems reach pressures of approximately 150 atmospheres before discharging and punching through the outer layer of the prey or predator at accelerations of more than 5 million g, making them one of the fastest biomechanical events known. To gain better understanding of the function of the complex, phylum-specific nematocyst organelle, and its venom payload, we compared the soluble nematocyst's proteome from the sea anemone Anemonia viridis, the jellyfish Aurelia aurita, and the hydrozoan Hydra magnipapillata, each belonging to one of the three basal cnidarian lineages which diverged over 600 Ma. Although the basic morphological and functional characteristics of the nematocysts of the three organisms are similar, out of hundreds of proteins identified in each organism, only six are shared. These include structural proteins, a chaperone which may help maintain venon activity over extended periods, and dickkopf, an enigmatic Wnt ligand which may also serve as a toxin. Nevertheless, many protein domains are shared between the three organisms' nematocyst content suggesting common proteome functionalities. The venoms of Hydra and Aurelia appear to be functionally similar and composed mainly of cytotoxins and enzymes, whereas the venom of the Anemonia is markedly unique and based on peptide neurotoxins. Cnidarian venoms show evidence for functional recruitment, yet evidence for diversification through positive selection, common to other venoms, is lacking. The final injected nematocyst payload comprises a mixture of dynamically evolving proteins involved in the development, maturation, maintenance, and discharge of the nematocysts, which is unique to each organism and potentially to each nematocyst type.

Tissue-Specific Venom Composition and Differential Gene Expression in Sea Anemones

“…We did not find any of the 167 nonactiniarian cnidarian toxin sequences in the transcriptomes of our focal taxa. This corroborated previous investigations into lineage-specific venom compositions among cnidarians (Rachamim et al 2014). …”

“…Of the better studied sea anemone toxin genes, voltage-gated sodium channel toxins (NaTxs) and type I and III voltage-gated potassium channel toxins (KTxs) appear to be specific to Actiniaria, with pore forming cytolysins found throughout Cnidaria (Frazao et al 2012). Many of the poorly studied toxin candidates are members of large gene families and share a strong resemblance to their nonvenomous counterparts (Fry et al 2009; Moran et al 2013; Rachamim et al 2014) or have been characterized in only one or two species (Frazao et al 2012). Previous tissue-specific investigations focusing on venom assays of crude extracts or isolated proteins have found that nematocyst type and abundance do not always correlate with venom potency (Hessinger 1988; Nevalainen et al 2004), that tissues thought to be devoid of nematocysts also have high concentrations of venom (Mathias et al 1960), and that whole tissue extracts can contain more potent bioactive compounds when compared with isolated peptides (Hessinger and Lenhoff 1976).…”

Corals hosting symbiotic hydrozoans are less susceptible to predation and disease

“…Coral-associated hydrozoans possess specialized polyp morphologies (called 'dactylozoids') dedicated exclusively to defend the colony [17], which are armed with venomous nematocysts capable of injecting a substance whose composition is substantially different from that released by anthozoans [29]. Furthermore, studies on related groups suggest that coralassociated hydrozoans may be hardly palatable due to noxious secondary metabolites, which could provide them with an additional, chemical defense against predators [30].…”

The nematocyst's sting is driven by the tubule moving front

“…Tentacles from the jellyfish Rhopilema nomadica [14] were collected from Haifa Bay, Israel, and their large isorhiza nematocysts were isolated as described in Rachamim et al [3] and activated with 1% subtilisin (Sigma). The nematocysts were trapped, activated and their elongation was measured in a microfluidic platform that was specially designed for this study (figure 1).…”