Abstract
BackgroundThe use of venom in intraspecific aggression is uncommon and venom-transmitting structures specifically used for intraspecific competition are found in few lineages of venomous taxa. Next-generation transcriptome sequencing allows robust characterization of venom diversity and exploration of functionally unique tissues. Using a tissue-specific RNA-seq approach, we investigate the venom composition and gene ontology diversity of acrorhagi, specialized structures used in intraspecific competition, in aggressive and non-aggressive polyps of the aggregating sea anemone Anthopleura elegantissima (Cnidaria: Anthozoa: Hexacorallia: Actiniaria: Actiniidae).ResultsCollectively, we generated approximately 450,000 transcripts from acrorhagi of aggressive and non-aggressive polyps. For both transcriptomes we identified 65 candidate sea anemone toxin genes, representing phospholipase A2s, cytolysins, neurotoxins, and acrorhagins. When compared to previously characterized sea anemone toxin assemblages, each transcriptome revealed greater within-species sequence divergence across all toxin types. The transcriptome of the aggressive polyp had a higher abundance of type II voltage gated potassium channel toxins/Kunitz-type protease inhibitors and type II acrorhagins. Using toxin-like proteins from other venomous taxa, we also identified 612 candidate toxin-like transcripts with signaling regions, potentially unidentified secretory toxin-like proteins. Among these, metallopeptidases and cysteine rich (CRISP) candidate transcripts were in high abundance. Furthermore, our gene ontology analyses identified a high prevalence of genes associated with “blood coagulation” and “positive regulation of apoptosis”, as well as “nucleoside: sodium symporter activity” and “ion channel binding”. The resulting assemblage of expressed genes may represent synergistic proteins associated with toxins or proteins related to the morphology and behavior exhibited by the aggressive polyp.ConclusionWe implement a multifaceted approach to investigate the assemblage of expressed genes specifically within acrorhagi, specialized structures used only for intraspecific competition. By combining differential expression, phylogenetic, and gene ontology analyses, we identify several candidate toxins and other potentially important proteins in acrorhagi of A. elegantissima. Although not all of the toxins identified are used in intraspecific competition, our analysis highlights some candidates that may play a vital role in intraspecific competition. Our findings provide a framework for further investigation into components of venom used exclusively for intraspecific competition in acrorhagi-bearing sea anemones and potentially other venomous animals.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1417-4) contains supplementary material, which is available to authorized users.
Highlights
The use of venom in intraspecific aggression is uncommon and venom-transmitting structures used for intraspecific competition are found in few lineages of venomous taxa
Each transcriptome was subjected to a suite of analyses to investigate the diversity of toxin-like sequences and overall gene ontology within acrorhagi of aggressive and nonaggressive polyps (Figure 2)
We used transcriptomes of the acrorhagi from aggressive and non-aggressive polyps of the sea anemone A. elegantissima to investigate the venom proteins and peptides in a tissue used in intraspecific competition
Summary
The use of venom in intraspecific aggression is uncommon and venom-transmitting structures used for intraspecific competition are found in few lineages of venomous taxa. Using a tissue-specific RNA-seq approach, we investigate the venom composition and gene ontology diversity of acrorhagi, specialized structures used in intraspecific competition, in aggressive and non-aggressive polyps of the aggregating sea anemone Anthopleura elegantissima (Cnidaria: Anthozoa: Hexacorallia: Actiniaria: Actiniidae). Sea anemones are unique among venomous animals, as many species participate in intraspecific aggressive encounters using specialized structures to transmit venom [4,5,6,7]. The acrorhagi inflate and adhere to the opponent (Figure 1), leaving an acrorhagial peel on the opponent [9]. The whitish peel, aggressor’s acrorhagi adhering to the victim (Figure 1), is surrounded by necrotic tissue [10]
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