Venom Gland Transcriptomic and Proteomic Analyses of the Enigmatic Scorpion Superstitionia donensis (Scorpiones: Superstitioniidae), with Insights on the Evolution of Its Venom Components
"> Figure 1
<p>(<b>A</b>) Distribution of annotated sequences from the venom gland transcriptome of <span class="html-italic">S. donensis</span> according to Gene Ontology (GO) terms. The category designated by GO as “Biological process” was the most diverse. (<b>B</b>–<b>D</b>) Distribution of the most represented categories within each GO term (GO numbers shown).</p> "> Figure 2
<p>Relative proportion (expressed as percentages) of the Pfam domains of the 135 annotated transcripts, which putatively code for venom components found in the venom gland transcriptome analysis of <span class="html-italic">S. donensis</span>. The category Toxins includes putative Na<sup>+</sup>, K<sup>+</sup> and Ca<sup>2+</sup> toxin channels peptides; the category NDBPs (Non-Disulfide-Bridged Peptides) includes all possible NDBPs peptides even when no Pfam domain was found; the category Protease Inhibitors includes Ascaris-Type and Kunitz-Type inhibitors; the category La1 includes putative La1-type peptides; the category Enzymes includes all possible peptides with venom enzymatic activity; and the category Other Venom Components includes putative venom proteins and possible CAP peptides.</p> "> Figure 3
<p>Sequence alignment of components with identity with sodium channel toxins (cysteine-stabilized α/β motif, CS αβ, indicated as CSab in the toxin names) found in the transcriptome analysis of the venom gland of <span class="html-italic">S. donensis</span> and those that were similar. Unitprot entry numbers precede the toxins’ names: (a) Component sdc14319_g1_i1, translated ORF; (b) CSab-Cer-2 from <span class="html-italic">Ce. squama</span>; (c) CSab-Cer-1 from <span class="html-italic">Ce. squama</span>; (d) CSab-Uro-2 from <span class="html-italic">Urodacus manicatus</span>; and (e) CSab-Iso-3 from <span class="html-italic">Isometroides vescus</span>.</p> "> Figure 4
<p>Amino acid sequences of the translated transcripts showing identity with the αKTx subfamily 6, found in the transcriptome analysis of the venom gland of <span class="html-italic">S. donensis</span>, aligned to similar sequences. Unitprot entry numbers precede the species’ names: C5J896 (potassium channel toxin αKTx 6.16); H2CYS1 (αKTx-like peptide); Q6XLL6 (potassium channel toxin αKTx 6.9); Q6XLL5 (Potassium channel toxin αKTx 6.10); Q6XLL7 (potassium channel toxin αKTx 6.8); Q6XLL8 (Potassium channel toxin αKTx 6.7); and P0DL37 (potassium channel toxin αKTx 6.21). The predicted signal peptide is underlined and the mature peptide is in bold.</p> "> Figure 5
<p>Sequence alignment of components with identity with Scorpines found in the transcriptome analysis of the venom gland of <span class="html-italic">S. donensis</span>. Peptide sequences were generated by translation from the reported transcripts. For comparative purposes, other known sequences are included (Unitprot entry numbers in brackets). Components sdc34997_g1_i1, sdc14222_g4_i1 and sdc14222_g4_i2; Hge scorpine and He scorpine-like 2 from <span class="html-italic">Ho. gertschi</span> (Q0GY40 and P0C8W5 respectively); Scorpine-like peptide Ev37 from <span class="html-italic">E. validus</span> (P0DL47); CSab-Cer-6 from <span class="html-italic">Ce. squama</span> (T1DMR0); β-KTx-like peptide LaIT2 from <span class="html-italic">Liocheles australasiae</span> (C7G3K3); Antimicrobial peptide scorpine-like 2 from <span class="html-italic">U. yaschenkoi</span> (L0GCW2); and Opiscorpine 3 from <span class="html-italic">Op. carinatus</span> (Q5WQZ7). The predicted signal peptide is underlined and the mature peptide is in bold.</p> "> Figure 6
<p>Sequence alignment of components with identity with calcins found in the transcriptome analysis of the venom gland of <span class="html-italic">S. donensis</span> and those that were similar. The transcripts were translated to generate the peptidic precursor sequences. Unitprot entry numbers in brackets. Components sdc9999_g2_i1 and sdc13987_g1_i1; Calcium channel toxin like 20 from <span class="html-italic">Urodacus yaschenkoi</span> (L0GBR1); Hadrucalcin from <span class="html-italic">Hoffmannihadrurus gertschi</span> (B8QG00); ViCaTx1 from <span class="html-italic">Thorellius intrepidus</span> [<a href="#B11-toxins-08-00367" class="html-bibr">11</a>]; β-KTx-like peptide LaIT2 from <span class="html-italic">Liocheles australasiae</span> (C7G3K3); Antimicrobial peptide scorpine-like 2 <span class="html-italic">Urodacus yaschenkoi</span> (L0GCW2); and Opiscorpine 3 from <span class="html-italic">Op. carinatus</span> (Q5WQZ7). The predicted signal peptide is underlined; the mature peptide is in bold and the propeptide is in italics.</p> "> Figure 7
<p>Sequence alignment of components with identity with Non-Disulfide-Bridged Peptides found in the transcriptome analysis of the venom gland of <span class="html-italic">S. donensis</span>. The sequences derived from transcripts were translated to show the precursor peptidic sequences. For comparative purposes other known sequences are included (Unitprot entry numbers in brackets): CYLIP-Uro-1 and CYLIP-Uro-3 from <span class="html-italic">U. manicatus</span> (T1E6X5 and T1DPA6, respectively); and CYLIP-Cer-2 and CYLIP-Cer-3 from <span class="html-italic">Ce. squama</span> (T1E6W7 and T1E7M2, respectively). The predicted signal peptide is underlined and the mature peptide is in bold.</p> "> Figure 8
<p>Phylogenetic tree obtained from the Bayesian analysis of 22 sequences of putative and confirmed calcins from 14 scorpion species belonging to 12 genera and eight families selected from the InterPro database and the available literature. The originally reported names are used (or the UniProt or GenBank accession codes for those lacking a name), followed by the scorpion species (see <a href="#app1-toxins-08-00367" class="html-app">Supplementary Table S3</a>). Posterior probabilities higher than 0.76 are indicated above the branches.</p> "> Figure 9
<p>Phylogenetic tree obtained from the Bayesian analysis of 62 sequences of scorpines and putative scorpines, plus 34 sequences of βKtx or putative βKtx from 34 scorpion species of 22 genera and 10 families, and one sequence as outgroup (αKTx), selected from the InterPro database and the available literature. Terminal names are composed of UniProt or GenBank accession codes and the name of the scorpion species, except for those named as in their original publications (see <a href="#app1-toxins-08-00367" class="html-app">Supplementary Table S4</a>). Posterior probabilities higher than 0.65 are indicated above/below branches. Clades in red represent sequences from species of genus <span class="html-italic">Tityus</span>; in light green sequences from species of genus <span class="html-italic">Mesobuthus</span>; in orange sequences from species of genus <span class="html-italic">Androctonus</span>; in magenta, sequences from species of genus <span class="html-italic">Chaerilus</span>; in yellow sequences from species of genus <span class="html-italic">Lychas</span>; in purple sequences from species of family Vaejovidae; in light blue sequences from species of family Scorpionidae; in dark green sequences from <span class="html-italic">S. donensis</span>, and in dark blue sequences from several non buthid families.</p> "> Figure 10
<p>Phylogenetic tree obtained from the Bayesian analysis of 36 sequences of La1-like peptides or putative La1-like peptides from 23 scorpion species of 18 genera and nine families selected from the InterPro database and the available literature. Terminal names are composed of UniProt or GenBank accession codes and the name of the scorpion species, except for those named as in their original publications (see <a href="#app1-toxins-08-00367" class="html-app">Supplementary Table S5</a>). Posterior probabilities higher than 0.65 are indicated above branches. Colored clades indicate monophyletic groups of La1-like peptides from scorpions of families Buthidae (red), Scorpionidae (green) and Vaejovidae (blue).</p> "> Figure 11
<p>Phylogenetic tree obtained from the Bayesian analysis of 20 sequences of potassium channel κ toxins (κKTxs) from eight scorpion species of four genera and three families; and 12 sequences of potassium channel α toxins and chlorotoxins as outgroup, selected from the InterPro database and available literature (see <a href="#app1-toxins-08-00367" class="html-app">Supplementary Table S6</a>). Posterior probabilities are indicated above branches. Colored clades indicate the monophyletic subfamilies proposed earlier: subfamily 1 (orange); subfamily 2 (blue); subfamily 3 (green); subfamily 4 (red); and subfamily 5 (purple). The name in red shows κ buthitoxin.</p> ">
Abstract
:1. Introduction
Calcins, Scorpines, La1-Like and Potassium Channel κ Toxins in Scorpion Venoms
2. Results and Discussion
2.1. S. donensis Venom Gland Global Transcriptomic Analysis
2.2. The Repertoire of Venom-Specific Transcripts in S. donensis
2.2.1. Toxins
Sodium Channel Toxins
Potassium channel toxins
Scorpine-like peptides
Calcins
2.2.2. Non-Disulfide-Bridged Peptides (NDBPs)
2.2.3. La1-Like Peptides
2.2.4. Enzymes
2.2.5. Protease Inhibitors
2.2.6. Other Venom Components
2.3. Amino Acid Sequence Determination of Venom Components
2.4. Phylogenetic Affinities of the Calcins, Scorpines, La1-Like Peptides and Potassium Channel κ Toxins Found in the Transcriptomic Analysis of the Venom Gland of S. donensis
2.4.1. Calcins
2.4.2. Scorpines
2.4.3. La1-Like Peptides
2.4.4. Potassium Channel κ Toxins (κKTx)
3. Conclusions
4. Materials and Methods
4.1. Biological Material
4.2. Molecular Mass Determination and Protein Identification
4.3. RNA Extraction, RNA-Seq and Venom Gland Transcriptome Assembly
4.4. Multiple Sequence Alignments, Phylogenetic Analysis and Motif Search
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Family | Venom Studies Available | cDNA or Transcriptome Analysis Available |
---|---|---|
Akravidae | No | No |
Bothriuridae | No | Yes |
Buthidae | Yes | Yes |
Caraboctonidae | Yes | Yes |
Chactidae | No | No |
Chaerilidae | Yes | Yes |
Diplocentridae | No | No |
Euscorpiidae | Under revision * | Under revision * |
Hemiscorpiidae | Yes | No |
Heteroscorpionidae | No | No |
Hormuridae | Yes | Yes |
Iuridae | No | No |
Pseudochactidae | No | No |
Scorpionidae | Yes | Yes |
Scorpiopidae | Yes | Yes |
Superstitioniidae | This study | This study |
Troglotayoscidae | No | No |
Typhlochactidae | No | No |
Urodacidae | Yes | Yes |
Vaejovidae | Yes | Yes |
Family | Calcins | Scorpines | La1-Like Peptides | Potassium Channel κ Toxins |
---|---|---|---|---|
Bothriuridae | No | Yes | Yes | No |
Buthidae | Yes | Yes | Yes | No |
Caraboctonidae | Yes | Yes | Yes | No |
Chaerilidae | Yes | Yes | Yes | No |
Hemiscorpiidae | No | No | No | No |
Hormuridae | No | Yes | Yes | Yes |
Scorpionidae | Yes | Yes | Yes | Yes |
Scorpiopidae | Yes | Yes | Yes | No |
Superstitioniidae | This study | This study | This study | This study |
Urodacidae | Yes | Yes | Yes | No |
Vaejovidae | Yes | Yes | Yes | Yes |
Peptide Type | Transcript | Score | # Unique Pep. | Seq. Cov. | MW (kDa) | Protein/Accession |
---|---|---|---|---|---|---|
NaTx | sdc14462_g1_i1 | 257.51 | 7 | 91.43% | 11.7 | Lipolysis activating peptide 1 alpha chain/93140443 |
sdc14462_g2_i2 | 29.7 | 2 | 29.81% | 11.8 | Birtoxin/20137305 | |
sdc15193_g1_i1 | 20.23 | 1 | 85.71% | 7.1 | Toxin Cll7/31376362 | |
sdc14462_g1_i2 | 118.64 | 1 | 78.10% | 11.8 | Altitoxin/116241245 | |
KTx | sdc13949_g1_i1 | 27.98 | 2 | 65.38% | 5.5 | Toxin KTx 8/159146538 |
sdc14273_g1_i2 | 58.09 | 1 | 76.32% | 4.1 | KTx 6.7/74838004 | |
Sc | sdc14222_g4_i1 | 296.09 | 3 | 86.90% | 9.3 | Hg scorpine like 2/224493299 |
sdc14222_g4_i2 | 153.55 | 3 | 76.47% | 9.2 | Hg scorpine like 2/224493299 | |
NDBP | sdc12606_g1_i1 | 59.38 | 2 | 50.00% | 4 | Vejovine/325515699 |
sdc14106_g1_i1 | 81.77 | 2 | 81.82% | 2.5 | Amp1/932534523 | |
sdc28695_g1_i1 | 45.7 | 2 | 77.27% | 2.4 | Amp2/932534537 | |
sdc4010_g1_i1 | 15.61 | 1 | 100.00% | 5.2 | Heterin 1/485896696 | |
sdc13544_g1_i1 | 83.11 | 1 | 86.79% | 6.4 | CYLIP Cer 2/522802549 | |
sdc14358_g5_i1 | 207.52 | 1 | 62.50% | 1.8 | Amphiphatic peptide CT2/384382524 | |
sdc14358_g12_i1 | 211.79 | 1 | 52.38% | 2.3 | CYLIP Cer 2/522802549 | |
sdc6540_g1_i1 | 161.85 | 1 | 52.38% | 2.3 | CYLIP Uro 3/522802596 | |
La1-like | sdc13004_g1_i1 | 111.52 | 4 | 92.68% | 9.1 | Putative secreted protein/240247657 |
sdc14036_g1_i1 | 162.81 | 2 | 100.00% | 8.4 | La1 like protein 15/430802826 | |
sdc12897_g1_i1 | 50.14 | 2 | 74.32% | 7.9 | La1 like protein 13/430802824 | |
sdc14589_g1_i1 | 53.02 | 1 | 90.24% | 8.8 | Toxin like protein 14/430802832 | |
Enzymes | sdc14619_g1_i3 | 310.92 | 9 | 87.73% | 67.7 | Neprilysin 1/567441193 |
sdc14393_g1_i1 | 70.24 | 4 | 76.13% | 26.4 | Phospholipase A2/218546750 | |
sdc14212_g1_i1 | 90.57 | 3 | 74.19% | 24.1 | Phospholipase A2/218546750 | |
sdc14619_g1_i1 | 42.67 | 1 | 78.17% | 83.3 | Neprilysin 1/567441193 | |
CAP | sdc3852_g1_i1 | 97.67 | 3 | 71.20% | 43.1 | CAP-Uro-1/522802590 |
sdc13900_g1_i1 | 87.21 | 2 | 54.10% | 38 | CAP-Iso-1/522802633 |
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Santibáñez-López, C.E.; Cid-Uribe, J.I.; Batista, C.V.F.; Ortiz, E.; Possani, L.D. Venom Gland Transcriptomic and Proteomic Analyses of the Enigmatic Scorpion Superstitionia donensis (Scorpiones: Superstitioniidae), with Insights on the Evolution of Its Venom Components. Toxins 2016, 8, 367. https://doi.org/10.3390/toxins8120367
Santibáñez-López CE, Cid-Uribe JI, Batista CVF, Ortiz E, Possani LD. Venom Gland Transcriptomic and Proteomic Analyses of the Enigmatic Scorpion Superstitionia donensis (Scorpiones: Superstitioniidae), with Insights on the Evolution of Its Venom Components. Toxins. 2016; 8(12):367. https://doi.org/10.3390/toxins8120367
Chicago/Turabian StyleSantibáñez-López, Carlos E., Jimena I. Cid-Uribe, Cesar V. F. Batista, Ernesto Ortiz, and Lourival D. Possani. 2016. "Venom Gland Transcriptomic and Proteomic Analyses of the Enigmatic Scorpion Superstitionia donensis (Scorpiones: Superstitioniidae), with Insights on the Evolution of Its Venom Components" Toxins 8, no. 12: 367. https://doi.org/10.3390/toxins8120367
APA StyleSantibáñez-López, C. E., Cid-Uribe, J. I., Batista, C. V. F., Ortiz, E., & Possani, L. D. (2016). Venom Gland Transcriptomic and Proteomic Analyses of the Enigmatic Scorpion Superstitionia donensis (Scorpiones: Superstitioniidae), with Insights on the Evolution of Its Venom Components. Toxins, 8(12), 367. https://doi.org/10.3390/toxins8120367