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The venom-gland transcriptome of the eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms.
BMC Genomics. 2013 Aug 02; 14:531.BG

Abstract

BACKGROUND

Snake venom is shaped by the ecology and evolution of venomous species, and signals of positive selection in toxins have been consistently documented, reflecting the role of venoms as an ecologically critical phenotype. New World coral snakes (Elapidae) are represented by three genera and over 120 species and subspecies that are capable of causing significant human morbidity and mortality, yet coral-snake venom composition is poorly understood in comparison to that of Old World elapids. High-throughput sequencing is capable of identifying thousands of loci, while providing characterizations of expression patterns and the molecular evolutionary forces acting within the venom gland.

RESULTS

We describe the de novo assembly and analysis of the venom-gland transcriptome of the eastern coral snake (Micrurus fulvius). We identified 1,950 nontoxin transcripts and 116 toxin transcripts. These transcripts accounted for 57.1% of the total reads, with toxins accounting for 45.8% of the total reads. Phospholipases A(2) and three-finger toxins dominated expression, accounting for 86.0% of the toxin reads. A total of 15 toxin families were identified, revealing venom complexity previously unknown from New World coral snakes. Toxins exhibited high levels of heterozygosity relative to nontoxins, and overdominance may favor gene duplication leading to the fixation of advantageous alleles. Phospholipase A(2) expression was uniformly distributed throughout the class while three-finger toxin expression was dominated by a handful of transcripts, and phylogenetic analyses indicate that toxin divergence may have occurred following speciation. Positive selection was detected in three of the four most diverse toxin classes, suggesting that venom diversification is driven by recurrent directional selection.

CONCLUSIONS

We describe the most complete characterization of an elapid venom gland to date. Toxin gene duplication may be driven by heterozygote advantage, as the frequency of polymorphic toxin loci was significantly higher than that of nontoxins. Diversification among toxins appeared to follow speciation reflecting species-specific adaptation, and this divergence may be directly related to dietary shifts and is suggestive of a coevolutionary arms race.

Authors+Show Affiliations

Department of Biological Science, Florida State University, Tallahassee, FL 32306-4295, USA.No affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

23915248

Citation

Margres, Mark J., et al. "The Venom-gland Transcriptome of the Eastern Coral Snake (Micrurus Fulvius) Reveals High Venom Complexity in the Intragenomic Evolution of Venoms." BMC Genomics, vol. 14, 2013, p. 531.
Margres MJ, Aronow K, Loyacano J, et al. The venom-gland transcriptome of the eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms. BMC Genomics. 2013;14:531.
Margres, M. J., Aronow, K., Loyacano, J., & Rokyta, D. R. (2013). The venom-gland transcriptome of the eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms. BMC Genomics, 14, 531. https://doi.org/10.1186/1471-2164-14-531
Margres MJ, et al. The Venom-gland Transcriptome of the Eastern Coral Snake (Micrurus Fulvius) Reveals High Venom Complexity in the Intragenomic Evolution of Venoms. BMC Genomics. 2013 Aug 2;14:531. PubMed PMID: 23915248.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The venom-gland transcriptome of the eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms. AU - Margres,Mark J, AU - Aronow,Karalyn, AU - Loyacano,Jacob, AU - Rokyta,Darin R, Y1 - 2013/08/02/ PY - 2013/02/19/received PY - 2013/07/29/accepted PY - 2013/8/7/entrez PY - 2013/8/7/pubmed PY - 2013/10/31/medline SP - 531 EP - 531 JF - BMC genomics JO - BMC Genomics VL - 14 N2 - BACKGROUND: Snake venom is shaped by the ecology and evolution of venomous species, and signals of positive selection in toxins have been consistently documented, reflecting the role of venoms as an ecologically critical phenotype. New World coral snakes (Elapidae) are represented by three genera and over 120 species and subspecies that are capable of causing significant human morbidity and mortality, yet coral-snake venom composition is poorly understood in comparison to that of Old World elapids. High-throughput sequencing is capable of identifying thousands of loci, while providing characterizations of expression patterns and the molecular evolutionary forces acting within the venom gland. RESULTS: We describe the de novo assembly and analysis of the venom-gland transcriptome of the eastern coral snake (Micrurus fulvius). We identified 1,950 nontoxin transcripts and 116 toxin transcripts. These transcripts accounted for 57.1% of the total reads, with toxins accounting for 45.8% of the total reads. Phospholipases A(2) and three-finger toxins dominated expression, accounting for 86.0% of the toxin reads. A total of 15 toxin families were identified, revealing venom complexity previously unknown from New World coral snakes. Toxins exhibited high levels of heterozygosity relative to nontoxins, and overdominance may favor gene duplication leading to the fixation of advantageous alleles. Phospholipase A(2) expression was uniformly distributed throughout the class while three-finger toxin expression was dominated by a handful of transcripts, and phylogenetic analyses indicate that toxin divergence may have occurred following speciation. Positive selection was detected in three of the four most diverse toxin classes, suggesting that venom diversification is driven by recurrent directional selection. CONCLUSIONS: We describe the most complete characterization of an elapid venom gland to date. Toxin gene duplication may be driven by heterozygote advantage, as the frequency of polymorphic toxin loci was significantly higher than that of nontoxins. Diversification among toxins appeared to follow speciation reflecting species-specific adaptation, and this divergence may be directly related to dietary shifts and is suggestive of a coevolutionary arms race. SN - 1471-2164 UR - https://www.unboundmedicine.com/medline/citation/23915248/The_venom_gland_transcriptome_of_the_eastern_coral_snake__Micrurus_fulvius__reveals_high_venom_complexity_in_the_intragenomic_evolution_of_venoms_ L2 - https://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-14-531 DB - PRIME DP - Unbound Medicine ER -