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Mar Drugs
2020 Aug 01;188:. doi: 10.3390/md18080407.
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Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus.
von Reumont BM
,
Lüddecke T
,
Timm T
,
Lochnit G
,
Vilcinskas A
,
von Döhren J
,
Nilsson MA
.
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Nemerteans (ribbon worms) employ toxins to subdue their prey, but research thus far has focused on the small-molecule components of mucus secretions and few protein toxins have been characterized. We carried out a preliminary proteotranscriptomic analysis of putative toxins produced by the hoplonemertean Amphiporus lactifloreus (Hoplonemertea, Amphiporidae). No variants were found of known nemertean-specific toxin proteins (neurotoxins, cytotoxins, parbolysins or nemertides) but several toxin-like transcripts were discovered, expressed strongly in the proboscis, including putative metalloproteinases and sequences resembling sea anemone actitoxins, crown-of-thorn sea star plancitoxins, and multiple classes of inhibitor cystine knot/knottin family proteins. Some of these products were also directly identified in the mucus proteome, supporting their preliminary identification as secreted toxin components. Two new nemertean-typical toxin candidates could be described and were named U-nemertotoxin-1 and U-nemertotoxin-2. Our findings provide insight into the largely overlooked venom system of nemerteans and support a hypothesis in which the nemertean proboscis evolved in several steps from a flesh-melting organ in scavenging nemerteans to a flesh-melting and toxin-secreting venom apparatus in hunting hoplonemerteans.
Figure 1. Habitus of Amphiporus lactifloreus (A) with a magnified stylet apparatus (B,C).
Figure 2. (A) Overview of toxin composition and identified putative toxin protein classes (outer circle) in the skin and mucus secretions of A. lactifloreus according to biological function (inner circle). The values reflect the percentage TPM (transcripts per million) values of transcripts grouped in the corresponding protein classes. (B) Bar chart showing the expression level for each transcript in TPM values (only transcripts identified by Mascot-based analysis (Table S2) are included).
Figure 3. Neighbor-joining network reconstruction of all identified nemertotoxin-1 (A) and nemertotoxin-2 (B) sequences in Splitstree 5 [37] with standard settings based on the uncorrected p-distances. A. lactifloreus and N. geniculatus sequences are shown in light and dark blue, respectively. Genus abbreviations for sea anemone taxa: Act = Actinia, Ane = Anemonia, Ant = Anthopleura, Ans = Antheopsis, Bun = Bundosoma, Con = Condylactis.
Figure 4. A cladogram illustrating the relationships among venomous, marine animal lineages (emphasis on nemerteans), showing the distribution of toxin protein classes. A green x indicates a known characterized toxin, a red x indicates proteotranscriptomic matches from A. lactifloreus, and a black x indicates toxin candidates supported by transcriptome data alone. The phylogeny is based on a recent genomics analysis [3]. Some lineages have been pruned for simplicity.
Figure 5. Model showing the evolutionary adaptations of toxin proteins and their expression in nemerteans with different feeding strategies. (A) A nemertean scavenger feeds on a fish carcass using the cocktail of proteases and other enzymes to macerate the tissue before ingestion, while toxins in the epidermis are used for defense. (B) A pilidiophoran that lacks a stylet apparatus captures a polychaete using paralytic toxins recruited into the proboscis. The proteases and other enzymes help the toxins reach their targets rapidly, and also facilitate a pre-digestion. (C) A hoplonemertean, such as A. lactifloreus, uses its venom apparatus to overpower an isopod crustacean with its prey-piercing stylet and toxins expressed in the proboscis.
Figure 6. Sampling strategy for the proteotranscriptomic analysis of A. lactifloreus shown with an everted proboscis. (A) The whole proboscis was used to scrape off secreted proteins and ultimately to generate transcriptome data. (B) The epidermis was sampled for secreted proteins. (C) The mucus around the whole animal was taken for proteome sample 3.
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