Transcriptomic Analysis of Four Cerianthid (Cnidaria, Ceriantharia) Venoms

Abstract

Tube anemones, or cerianthids, are a phylogenetically informative group of cnidarians with complex life histories, including a pelagic larval stage and tube-dwelling adult stage, both known to utilize venom in stinging-cell rich tentacles. Cnidarians are an entirely venomous group that utilize their proteinaceous-dominated toxins to capture prey and defend against predators, in addition to several other ecological functions, including intraspecific interactions. At present there are no studies describing the venom for any species within cerianthids. Given their unique development, ecology, and distinct phylogenetic-placement within Cnidaria, our objective is to evaluate the venom-like gene diversity of four species of cerianthids from newly collected transcriptomic data. We identified 525 venom-like genes between all four species. The venom-gene profile for each species was dominated by enzymatic protein and peptide families, which is consistent with previous findings in other cnidarian venoms. However, we found few toxins that are typical of sea anemones and corals, and furthermore, three of the four species express toxin-like genes closely related to potent pore-forming toxins in box jellyfish. Our study is the first to provide a survey of the putative venom composition of cerianthids and contributes to our general understanding of the diversity of cnidarian toxins.

Phylogenetic and Selection Analysis of an Expanded Family of Putatively Pore-Forming Jellyfish Toxins (Cnidaria: Medusozoa)

“…We identified 15 putative JFTs from ten species of anthozoans that passed our filtering criteria, including four recently reported sequences from three ceriantharian (tube anemones) species ( Klompen et al 2020 ). Preliminary phylogenetic analyses did not recover stable placement for the anthozoan sequences, with low bootstrap support for many of the clades and little discernable taxonomic patterns.…”

“…S2 and S3 , Supplementary Material online). To the best of our knowledge, predicted JFT-like genes from anthozoans have only been identified via genomic (e.g., Gacesa et al 2015 ) and transcriptomic studies (e.g., Rachamim et al 2015 ; Surm et al 2019 ; Klompen et al 2020 ), with no JFT-like peptides isolated from proteomic analyses that included anthozoan venoms (e.g., Rachamim et al 2015 ; Surm et al 2019 ). Given that current evidence does not support anthozoans possessing JFT-like toxins in their venoms, our study focused on medusozoan JFT-like candidates.…”

“…3 ). The scyphozoans in JFT-1c included a previously described Chrysaora fuscescens toxin, Cfus-TX1 ( Ponce et al 2016 ), two toxins from the polyps of Aurelia aurita (Linnaeus, 1785) (Toxin 1 and Toxin 2) ( The UniProt Consortium 2019 ), and a recently described toxin from Cassiopea xamachana (CassTX-B) ( Ames and Klompen et al 2020 ), as well as additional sequences from Aurelia spp. and C. nozakii .…”

“…Conversely, several species that lack representatives from the JFT-1b clade are also known to be toxic to vertebrates, including the scyphozoans C. nozakii ( Feng et al 2010 ) and C. fuscescens ( Ponce et al 2016 ). Instead, these relatively potent stingers have representatives in the JFT-1c clade along with less toxic species such as the moon jelly Aurelia and the upside-down jellyfish Cassiopea , although mucus released from Cassiopea is able to sting fish ( Stoner et al 2014 ) as well as humans ( Ames and Klompen et al 2020 ). This suggests that not all JFT-1 proteins are potent toxins or, alternatively, are not abundant enough within the delivered venom cocktail of these specific species to cause severe medical damage to humans.…”

“…( Rachamim et al 2015 ; Gold et al 2019 ), Cassiopea xamachana Bigelow, 1892 ( Ames, Klompen et al 2020 ), Cyanea capillata (Linnaeus, 1758) ( Lassen et al 2011 ), Nemopilema nomurai Kishinouye, 1922 ( Li et al 2014 as Stomolophus meleagris , Wang et al 2018 , but see Li et al 2020 ), and Chrysaora fuscescens Brandt, 1835 ( Ponce et al 2016 ), and the hydrozoan Hydra vulgaris Pallas, 1766 (as H. magnipapillata ) ( Balasubramanian et al 2012 ; Rachamim et al 2015 ) (see additional examples in supplementary table S1 , Supplementary Material online). Although a small number of predicted genes or transcripts of putative JFTs have been found in anthozoans ( Rachamim et al 2015 ; Gacesa et al 2015 ; Surm et al 2019 ; Klompen et al 2020 ), no matching peptides have been identified using proteomic analyses of extracted crude venom or tentacle tissue from this clade, casting doubt that these are true toxin-coding genes. The apparent restriction of JFTs to medusozoan venoms resulted in the current nomenclature of “jellyfish toxins” ( Jouiaei, Yanagihara, et al 2015 ), though several different names have been used over the last two decades ( table 1 ).…”