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Assembling an arsenal, the scorpion way.

Kozminsky-Atias A, Bar-Shalom A, Mishmar D, Zilberberg N - BMC Evol. Biol. (2008)

Bottom Line: Upon fixation, the mature toxin-coding domain was subjected to diversifying selection resulting in a significantly higher substitution rate that can be explained solely by diversifying selection.We interpret this as resulting from purifying selection acting on both the peptide and, as reported here for the first time, the DNA sequence, to create a toxin family-specific codon bias.We thus propose that scorpion toxin genes were shaped by selective forces acting at three levels, namely (1) diversifying the mature toxin, (2) conserving the leader peptide amino acid sequence and intriguingly, (3) conserving the leader DNA sequences.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel. adiko@bgu.ac.il

ABSTRACT

Background: For survival, scorpions depend on a wide array of short neurotoxic polypeptides. The venoms of scorpions from the most studied group, the Buthida, are a rich source of small, 23-78 amino acid-long peptides, well packed by either three or four disulfide bridges that affect ion channel function in excitable and non-excitable cells.

Results: In this work, by constructing a toxin transcripts data set from the venom gland of the scorpion Buthus occitanus israelis, we were able to follow the evolutionary path leading to mature toxin diversification and suggest a mechanism for leader peptide hyper-conservation. Toxins from each family were more closely related to one another than to toxins from other species, implying that fixation of duplicated genes followed speciation, suggesting early gene conversion events. Upon fixation, the mature toxin-coding domain was subjected to diversifying selection resulting in a significantly higher substitution rate that can be explained solely by diversifying selection. In contrast to the mature peptide, the leader peptide sequence was hyper-conserved and characterized by an atypical sub-neutral synonymous substitution rate. We interpret this as resulting from purifying selection acting on both the peptide and, as reported here for the first time, the DNA sequence, to create a toxin family-specific codon bias.

Conclusion: We thus propose that scorpion toxin genes were shaped by selective forces acting at three levels, namely (1) diversifying the mature toxin, (2) conserving the leader peptide amino acid sequence and intriguingly, (3) conserving the leader DNA sequences.

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Phylogenetic trees of the depressant toxin family of Boi and BmK scorpions. (A) Full transcript, (B) leader-coding domain and (C) mature-coding domain of depressant toxins from both Boi and BmK scorpions were aligned by the MUSCLE algorithm and edited manually with Jalview. Trees were constructed by the neighbor-joining method, based on maximum likelihood composite. Numbers on the branches are bootstrap percentages, while brackets mark the genus origin of the toxins. Boi transcripts are shadowed in blue.
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Figure 2: Phylogenetic trees of the depressant toxin family of Boi and BmK scorpions. (A) Full transcript, (B) leader-coding domain and (C) mature-coding domain of depressant toxins from both Boi and BmK scorpions were aligned by the MUSCLE algorithm and edited manually with Jalview. Trees were constructed by the neighbor-joining method, based on maximum likelihood composite. Numbers on the branches are bootstrap percentages, while brackets mark the genus origin of the toxins. Boi transcripts are shadowed in blue.

Mentions: An attempt to decipher the relative time frame in which gene duplication events led to toxin divergence was next undertaken. At this point in time, a transcript dataset of the venom gland content from only a single scorpion species, namely Buthus martensi Karsch (BmK), gradually obtained over the course of the last few years [16], was available. cDNA sequences coding for the depressant toxin families from the two scorpions, i.e. Boi and BmK, were thus aligned and a neighbor-joining tree was constructed (Fig. 2A). Unexpectedly, most sequences in both families are more similar to others from the same species than to any of the sequences of the other species. Similar pattern was observed for the α-toxin family (not shown). If speciation was linked only to the evolution of the mature toxin one would expect the disappearance of the segregation when only the leader-coding sequence is considered. When examining separately the phylogenetic trees of the mature and the leader-coding domains (Fig. 2B, C), the leader-coding domain seemed to segregate even earlier than the mature toxin-coding domain. This will be further elucidated in the Discussion. Thus, these data can be interpreted as indicating that the two species diverged from a common progenitor before the duplication and diversification of toxins from the two families had occurred.


Assembling an arsenal, the scorpion way.

Kozminsky-Atias A, Bar-Shalom A, Mishmar D, Zilberberg N - BMC Evol. Biol. (2008)

Phylogenetic trees of the depressant toxin family of Boi and BmK scorpions. (A) Full transcript, (B) leader-coding domain and (C) mature-coding domain of depressant toxins from both Boi and BmK scorpions were aligned by the MUSCLE algorithm and edited manually with Jalview. Trees were constructed by the neighbor-joining method, based on maximum likelihood composite. Numbers on the branches are bootstrap percentages, while brackets mark the genus origin of the toxins. Boi transcripts are shadowed in blue.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2651877&req=5

Figure 2: Phylogenetic trees of the depressant toxin family of Boi and BmK scorpions. (A) Full transcript, (B) leader-coding domain and (C) mature-coding domain of depressant toxins from both Boi and BmK scorpions were aligned by the MUSCLE algorithm and edited manually with Jalview. Trees were constructed by the neighbor-joining method, based on maximum likelihood composite. Numbers on the branches are bootstrap percentages, while brackets mark the genus origin of the toxins. Boi transcripts are shadowed in blue.
Mentions: An attempt to decipher the relative time frame in which gene duplication events led to toxin divergence was next undertaken. At this point in time, a transcript dataset of the venom gland content from only a single scorpion species, namely Buthus martensi Karsch (BmK), gradually obtained over the course of the last few years [16], was available. cDNA sequences coding for the depressant toxin families from the two scorpions, i.e. Boi and BmK, were thus aligned and a neighbor-joining tree was constructed (Fig. 2A). Unexpectedly, most sequences in both families are more similar to others from the same species than to any of the sequences of the other species. Similar pattern was observed for the α-toxin family (not shown). If speciation was linked only to the evolution of the mature toxin one would expect the disappearance of the segregation when only the leader-coding sequence is considered. When examining separately the phylogenetic trees of the mature and the leader-coding domains (Fig. 2B, C), the leader-coding domain seemed to segregate even earlier than the mature toxin-coding domain. This will be further elucidated in the Discussion. Thus, these data can be interpreted as indicating that the two species diverged from a common progenitor before the duplication and diversification of toxins from the two families had occurred.

Bottom Line: Upon fixation, the mature toxin-coding domain was subjected to diversifying selection resulting in a significantly higher substitution rate that can be explained solely by diversifying selection.We interpret this as resulting from purifying selection acting on both the peptide and, as reported here for the first time, the DNA sequence, to create a toxin family-specific codon bias.We thus propose that scorpion toxin genes were shaped by selective forces acting at three levels, namely (1) diversifying the mature toxin, (2) conserving the leader peptide amino acid sequence and intriguingly, (3) conserving the leader DNA sequences.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Life Sciences, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel. adiko@bgu.ac.il

ABSTRACT

Background: For survival, scorpions depend on a wide array of short neurotoxic polypeptides. The venoms of scorpions from the most studied group, the Buthida, are a rich source of small, 23-78 amino acid-long peptides, well packed by either three or four disulfide bridges that affect ion channel function in excitable and non-excitable cells.

Results: In this work, by constructing a toxin transcripts data set from the venom gland of the scorpion Buthus occitanus israelis, we were able to follow the evolutionary path leading to mature toxin diversification and suggest a mechanism for leader peptide hyper-conservation. Toxins from each family were more closely related to one another than to toxins from other species, implying that fixation of duplicated genes followed speciation, suggesting early gene conversion events. Upon fixation, the mature toxin-coding domain was subjected to diversifying selection resulting in a significantly higher substitution rate that can be explained solely by diversifying selection. In contrast to the mature peptide, the leader peptide sequence was hyper-conserved and characterized by an atypical sub-neutral synonymous substitution rate. We interpret this as resulting from purifying selection acting on both the peptide and, as reported here for the first time, the DNA sequence, to create a toxin family-specific codon bias.

Conclusion: We thus propose that scorpion toxin genes were shaped by selective forces acting at three levels, namely (1) diversifying the mature toxin, (2) conserving the leader peptide amino acid sequence and intriguingly, (3) conserving the leader DNA sequences.

Show MeSH
Related in: MedlinePlus