Are Fireworms Venomous? Evidence for the Convergent Evolution of Toxin Homologs in Three Species of Fireworms (Annelida, Amphinomidae)

Abstract

Amphinomids, more commonly known as fireworms, are a basal lineage of marine annelids characterized by the presence of defensive dorsal calcareous chaetae, which break off upon contact. It has long been hypothesized that amphinomids are venomous and use the chaetae to inject a toxic substance. However, studies investigating fireworm venom from a morphological or molecular perspective are scarce and no venom gland has been identified to date, nor any toxin characterized at the molecular level. To investigate this question, we analyzed the transcriptomes of three species of fireworms—Eurythoe complanata, Hermodice carunculata, and Paramphinome jeffreysii—following a venomics approach to identify putative venom compounds. Our venomics pipeline involved de novo transcriptome assembly, open reading frame, and signal sequence prediction, followed by three different homology search strategies: BLAST, HMMER sequence, and HMMER domain. Following this pipeline, we identified 34 clusters of orthologous genes, representing 13 known toxin classes that have been repeatedly recruited into animal venoms. Specifically, the three species share a similar toxin profile with C-type lectins, peptidases, metalloproteinases, spider toxins, and CAP proteins found among the most highly expressed toxin homologs. Despite their great diversity, the putative toxins identified are predominantly involved in three major biological processes: hemostasis, inflammatory response, and allergic reactions, all of which are commonly disrupted after fireworm stings. Although the putative fireworm toxins identified here need to be further validated, our results strongly suggest that fireworms are venomous animals that use a complex mixture of toxins for defense against predators.

New Evidence of Marine Fauna Tropicalization off the Southwestern Iberian Peninsula (Southwest Europe)

“…This species may pose public health risks if it becomes abundant off the Algarve coast, since its calcareous chaetae induce intense pain, inflammation, and edema when they come into contact with human skin. It is important to mention that there is no agreement on classifying this species as venomous, poisonous, or toxic [33]. Nevertheless, precautionary measures should be implemented to prevent people from touching this species if it becomes widespread, especially in highly tourist regions such as the Algarve.…”

New Evidence of Marine Fauna Tropicalization off the Southwestern Iberian Peninsula

“…However, the venomous stings of bearded fireworm may raise a public health concern if this species becomes abundant in the Algarve coast. The calcareous chaetae present alongside the body deliver numerous toxins that cause intense pain, inflammation, and edema when in contact with human skin, alongside with neurotoxins that can cause localized paresthesia and numbness [33]. So, precautionary measures should be implemented to prevent people of touching this species if it becomes widespread, especially in highly touristic regions as the Algarve.…”

Studying Smaller and Neglected Organisms in Modern Evolutionary Venomics Implementing RNASeq (Transcriptomics)—A Critical Guide

“…As a consequence, methodological limitations often occur that demand an assessment on how they might impact on the addressed hypotheses of venom evolution in the respective, neglected taxon. In particular, if one main (or even sometimes only [ 40 , 41 ]) strategy is to rely on transcriptomics, subsequent conclusions need to be drawn carefully. This article provides a very generalized “template” processing flow for RNASeq analyses in evolutionary venomics with a focus on smaller neglected organisms and related methodological issues that can be adapted for own project strategies.…”