Abstract
To date, few studies have been carried out aimed at characterizing the toxins synthesized by hydrocorals of the genus Millepora. The purpose of this study was to explore the toxin diversity and antibacterial activity of the “fire coral” M. complanata using a transcriptomic data mining approach. In addition, the cytolytic and antibacterial activities of the M. complanata nematocyst proteome were experimentally confirmed. Cytolysins were predicted from the transcriptome by comparing against the Animal Toxin Annotation Project database, resulting in 190 putative toxins, including metalloproteases, hemostasis-impairing toxins, phospholipases, among others. The M. complanata nematocyst proteome was analyzed by 1D and 2D electrophoresis and zymography. The zymograms showed different zones of cytolytic activity: two zones of hemolysis at ~25 and ~205 kDa, two regions corresponding to phospholipase A2 (PLA2) activity around 6 and 25 kDa, and a proteolytic zone was observed between 50 and 205 kDa. The hemolytic activity of the proteome was inhibited in the presence of PLA2 and proteases inhibitors, suggesting that PLA2s, trypsin, chymotrypsin, serine-proteases, and matrix metalloproteases are responsible for the hemolysis. On the other hand, antimicrobial peptide sequences were retrieved from their transcripts with the amPEPpy software. This analysis revealed the presence of homologs to SK84, cgUbiquitin, Ubiquicidin, TroTbeta4, SPINK9-v1, and Histone-related antimicrobials in the transcriptome of this cnidarian. Finally, by employing disk diffusion and microdilution assays, we found that the nematocyst peptidome of M. complanata showed inhibitory activity against both Gram-positive and Gram-negative bacteria including S. enteritidis, P. perfectomarina, E. coli, and C. xerosis, among others. This is the first transcriptomic data mining analysis to explore the diversity of the toxins synthesized by an organism of the genus Millepora. Undoubtedly, this work provides information that will broaden our general understanding of the structural richness of cnidarian toxins.
Highlights
Cnidarians are simple and ancestral organisms considered as the oldest lineage of poisonous animals, which have the ability to synthesize molecules capable of inducing different toxic effects and lethality [1]
These complex chemical mixtures contain mainly peptidic and proteinaceous components, which have been categorized into three principal groups, based on their mechanism of action: (a) enzymes (e.g., metalloproteases and phospholipases A2 (PLA2s)) [1,3]; (b) pore-forming toxins (PFTs) (e.g., actinoporins, jellyfish toxins (JFTs), hydralysins (Hlns), etc.) [4]; and (c) neurotoxins (e.g., toxins that target voltage-gated sodium channels (NaTXs), toxins targeting voltage-gated potassium channels (KTXs), Kunitz peptides, etc.)
We explored the toxin diversity synthesized by the “fire coral” M. complanata and predicted the presence of antimicrobial peptides by using a transcriptome data mining approach
Summary
Cnidarians are simple and ancestral organisms considered as the oldest lineage of poisonous animals, which have the ability to synthesize molecules capable of inducing different toxic effects and lethality [1]. Cnidarian venoms are stored in the nematocysts, specialized organelles for defense and prey capture [2] These complex chemical mixtures contain mainly peptidic and proteinaceous components, which have been categorized into three principal groups, based on their mechanism of action: (a) enzymes (e.g., metalloproteases and phospholipases A2 (PLA2s)) [1,3]; (b) pore-forming toxins (PFTs) (e.g., actinoporins, jellyfish toxins (JFTs), hydralysins (Hlns), etc.) [4]; and (c) neurotoxins (e.g., toxins that target voltage-gated sodium channels (NaTXs), toxins targeting voltage-gated potassium channels (KTXs), Kunitz peptides, etc.) [5]. Cnidarian toxins possess a wide spectrum of biological effects, for instance, PLA2s hydrolyze the sn-2 ester bond of glycerophospholipids producing lysophospholipids and fatty acids [7]. These toxins display other pharmacological effects, such as neurotoxicity [8]
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