Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus
Abstract
:1. Introduction
2. Results
2.1. No Nemertean-Specific Toxin Transcripts Are Present in the A. lactifloreus Proboscis Transcriptome
2.2. Metalloproteinase M12 and Actitoxin-Like Transcripts Are the Most Abundant Putative Toxin Transcripts in the Proboscis of A. lactifloreus
2.3. Proteinases Dominate the Skin and Mucus Secretions Accompanied by Mucins, Enzymes and Putative Toxins
2.4. Several Secreted Proteins Are Strongly Expressed but Remain Mostly Uncharacterized
2.5. No Putative Antimicrobial Peptides Were Identified in the A. lactifloreus Proteotranscriptome
3. Discussion
3.1. Are Known Nemertean Toxins Taxon-Specific?
3.2. The Putative Venom Cocktail of A. lactifloreus and Its Mode of Action
3.3. General Use of Toxin Proteins and Their Mode of Action in Nemerteans
4. Conclusions
5. Materials and Methods
5.1. Collection and Preparation of A. lactifloreus Specimens
5.2. RNA Isolation, Library Preparation and Illumina Sequencing
5.3. Transcriptome Assembly, ORF Prediction and Identification of Venom Proteins
5.4. Peptide and Protein Identification
5.5. Matching Proteome and Transcriptome Data
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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ToxProt Annotation | Protein Family, “Actual” Scaffold | Original Taxon Source | Presumed Activity | Transcripts Included/(All) | Expression TPMs (Sum) |
---|---|---|---|---|---|
Toxin Candidates | |||||
Actitoxin-like* (Nemertotoxin 2) | Actitoxins, Kunitz-BPTI | Sea anemones | Possible neurotoxicity | 10/(32) | 1052.76 |
Delta-actitoxin-like | Actitoxins, Kunitz-BPTI | Sea anemones | Possible neurotoxicity | 2/(2) | 134.56 |
Conotoxin-like | Conotoxin-like ICK 4-C scaffold | Mollusks | Possible neurotoxicity | 1/(3) | 19.74 |
Conotoxin-like | Xibalbin1-like ICK 8-C scaffold | Mollusks | Possible neurotoxicity | 2/(3) | 19.74 |
Plancitoxin-like* (Nemertotoxin 1) | DNase II | Starfishes | Possible hepatotoxicity | 7/(7) | 29.17 |
Putative calcium channel toxin Tx758-like | ICK, knottin cysteine rich | Scorpions | Possible neurotoxicity | 1/(1) | 85.10 |
Kunitz-type U1 aranetoxin-like | Kunitz-BPTI, cysteine-rich | Spiders | Possible neurotoxicity | 1/(1) | 9.42 |
Proteinase Candidates | |||||
Astacin-like metalloproteinase* | Metalloproteinase M12A | Diverse species | Proteinase activity | 8/(52) | 2597.43 |
Nematocyst expressed protein 6 | Metalloproteinase M12A | Cnidarians | Proteinase activity | 1/(36) | 29.92 |
Metalloproteinase zinc-disintegrin | Metalloproteinase ADAM | Diverse species | Proteinase activity | 1/(23) | 0.07 |
Enzyme Candidates | |||||
Venom allergen 5 | CAP, Cysteine-rich | Diverse species | Enzymatic | 1/(5) | 1.76 |
C-type lectin (lectotoxin) | Lectins, C-type lectin | Diverse species | Enzymatic | 3/(14) | 5.5 |
Galactose-specific lectin* (nattectin) | Lectins, C-type lectin | Diverse species | Enzymatic | 2/(11) | 3.20 |
Calglandulin* | Calglandulins, EF-hand motif | Diverse species | Enzymatic | 3/(75) | 8.58 |
Cysteine-rich protein | Diverse, cysteine-rich | Diverse species | Enzymatic | 2/(25) | 16.89 |
Hyaluronidase (Conhyal-Cn1) | Hyaluronidase | Diverse species | Enzymatic | 6/(9) | 10.68 |
Kunitz-type serine proteinase inhibitor | Serpin | Diverse species | Enzymatic | 3/(3) | 20.81 |
Phospholipase A2 | Phospholipase A2 | Diverse species | Enzymatic | 4/(6) | 713.59 |
Snaclec bitiscetin | Lectins | Diverse species | Enzymatic | 4/(5) | 4.38 |
Snaclec coagulation factor | Lectins | Diverse species | Enzymatic | 3/(4) | 3.05 |
Snake venom metalloproteinase inhibitor | SVMP | Diverse species | Proteinase activity | 3/(7) | 8.15 |
Snake venom 5 nucleotidase | 5-Nuclease | Snakes | Proteinase activity | 3/(4) | 15.43 |
Other Protein Candidates | |||||
Vascular endothelial growth factor | Growth factors | Diverse species | Possible spreading factor | 1/(2) | 4.42 |
Venom nerve growth factor | Growth factors | Diverse species | Possible spreading factor | 1/(2) | 10.16 |
Insulin-like growth factor (IGFVB) | Growth factors | Diverse species | Possible spreading factor | 3/(49) | 3 |
Neuropeptide prohormone-4 | Hormone precursor | Diverse species | Possible spreading factor | 2/(7) | 155.35 |
Transcript | TPM Value | Mascot Score | Length (aa) | Signal Peptide | Scaffold/Domain Prediction (Sequence Residue) |
---|---|---|---|---|---|
DN187_c0_g1_i14.p1 | 8524.05 | 195 | 161 | yes (1–17) | Non-cytoplasmic domain (18–160), disorder prediction (137–160) |
DN66444_c0_g1_i1.p1 | 2276.01 | 117 | 144 | yes (1–19) | Non-cytoplasmic domain (20–144) |
DN2243_c0_g1_i6.p1 | 2243.13 | 104 | 158 | yes (1–22) | Non-cytoplasmic domain (23–158) |
DN904_c0_g1_i1.p1 | 1328.59 | 177 | 100 | yes (1–18) | Non-cytoplasmic domain (19–100) |
DN416_c0_g1_i1.p1 | 1173.91 | 70 | 198 | yes (1–19) | Non-cytoplasmic domain (20–198) |
DN2192_c0_g1_i1.p1 | 709.61 | 114 | 117 | yes (1–20) | Non-cytoplasmic domain (21–116) |
DN4062_c0_g1_i1.p1 | 558.79 | 60 | 210 | yes (1–23) | Non-cytoplasmic domain (24–210) |
DN629_c0_g1_i1.p1 | 513.04 | 48 | 117 | yes (1–43) | Non-cytoplasmic domain (44–117) |
DN4200_c0_g1_i1.p1 | 394.49 | 101 | 122 | yes (1–22) | Non-cytoplasmic domain (23–122), disorder prediction (20–108) |
DN1209_c0_g2_i1.p1 | 143.95 | 62 | 309 | yes (1–16) | Non cytoplasmic domain (17–308), disorder prediction (26–135), proline rich |
DN5_c1_g1_i1.p1 | 140.00 | 78 | 117 | no | Disorder prediction, coil (54–74) |
DN355_c0_g1_i1.p1 | 36.43 | 30 | 107 | yes (1–34) | Non-cytoplasmic domain (15–107), disorder prediction (38–65) |
DN21169_c0_g1_i1.p1 | 6.28 | 95 | 120 | yes (1–20) | Non-cytoplasmic domain (21–119) |
DN5485_c1_g1_i2.p1 | 6.13 | 150 | 121 | no | Galactose-like binding sf, unknown (11–120) |
DN646_c1_g1_i1.p1 | 3.93 | 25 | 330 | yes (1–20) | Non-cytoplasmic domain (21–330), disorder prediction (121–143), EGGSHELL |
DN9918_c0_g1_i1.p1 | 3.40 | 239 | 204 | yes (1–18) | Non-cytoplasmic domain (19203–), Unknown (25–177) |
DN68091_c0_g1_i1.p1 | 3.28 | 137 | 121 | no | Unknown unintegrated (41–113) |
DN11320_c0_g1_i1.p1 | 2.83 | 280 | 113 | yes (1–17) | Non-cytoplasmic domain (18–113) |
DN70554_c0_g1_i1.p1 | 2.80 | 305 | 112 | no | Disorder prediction (1–25) |
DN39869_c0_g1_i1.p1 | 2.30 | 146 | 157 | yes (1–17) | Non-cytoplasmic domain (18–157) |
DN8497_c0_g1_i1.p2 | 2.16 | 60 | 131 | yes (1–23) | Non-cytoplasmic domain (24–131) |
DN16202_c0_g2_i1.p1 | 2.07 | 223 | 279 | no | NA, proline and cysteine rich, disorder prediction (101–139) |
DN40599_c0_g1_i1.p1 | 1.79 | 65 | 152 | NA | NA |
DN7825_c0_g1_i1.p1 | 1.66 | 176 | 223 | no | Non-cytoplasmic domain (37–222) |
DN16202_c0_g1_i1.p1 | 1.52 | 461 | 282 | no | NA, proline and cysteine rich |
DN40858_c0_g1_i1.p1 | 1.36 | 47 | 167 | NA | NA |
DN78568_c0_g1_i1.p1 | 1.28 | 99 | 146 | no | Non-cytoplasmic domain (22–97) |
DN60477_c0_g1_i1.p1 | 1.11 | 44 | 169 | no | Unknown integrated (1-121), cysteine rich |
DN7590_c0_g1_i1.p1 | 0.99 | 278 | 168 | no | Unknown unintegrated (1–121) |
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von Reumont, B.M.; Lüddecke, T.; Timm, T.; Lochnit, G.; Vilcinskas, A.; von Döhren, J.; Nilsson, M.A. Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus. Mar. Drugs 2020, 18, 407. https://doi.org/10.3390/md18080407
von Reumont BM, Lüddecke T, Timm T, Lochnit G, Vilcinskas A, von Döhren J, Nilsson MA. Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus. Marine Drugs. 2020; 18(8):407. https://doi.org/10.3390/md18080407
Chicago/Turabian Stylevon Reumont, Björn Marcus, Tim Lüddecke, Thomas Timm, Günter Lochnit, Andreas Vilcinskas, Jörn von Döhren, and Maria A. Nilsson. 2020. "Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus" Marine Drugs 18, no. 8: 407. https://doi.org/10.3390/md18080407