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RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes

BACKGROUND: Largely because of their direct, negative impacts on human health, the venoms of front-fanged snakes of the families Viperidae and Elapidae have been extensively characterized proteomically, transcriptomically, and pharmacologically. However, relatively little is known about the molecula...

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Autores principales: McGivern, James J, Wray, Kenneth P, Margres, Mark J, Couch, Michelle E, Mackessy, Stephen P, Rokyta, Darin R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4289226/
https://www.ncbi.nlm.nih.gov/pubmed/25476704
http://dx.doi.org/10.1186/1471-2164-15-1061
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author McGivern, James J
Wray, Kenneth P
Margres, Mark J
Couch, Michelle E
Mackessy, Stephen P
Rokyta, Darin R
author_facet McGivern, James J
Wray, Kenneth P
Margres, Mark J
Couch, Michelle E
Mackessy, Stephen P
Rokyta, Darin R
author_sort McGivern, James J
collection PubMed
description BACKGROUND: Largely because of their direct, negative impacts on human health, the venoms of front-fanged snakes of the families Viperidae and Elapidae have been extensively characterized proteomically, transcriptomically, and pharmacologically. However, relatively little is known about the molecular complexity and evolution of the venoms of rear-fanged colubrid snakes, which are, with a few notable exceptions, regarded as harmless to humans. Many of these snakes have venoms with major effects on their preferred prey, and their venoms are probably as critical to their survival as those of front-fanged elapids and viperids. RESULTS: We sequenced the venom-gland transcriptomes from a specimen of Hypsiglena (Desert Night Snake; family Colubridae, subfamily Dipsadinae) and of Boiga irregularis (Brown Treesnake; family Colubridae, subfamily Colubrinae) and verified the transcriptomic results proteomically by means of high-definition mass spectrometry. We identified nearly 3,000 nontoxin genes for each species. For B. irregularis, we found 108 putative toxin transcripts in 46 clusters with <1% nucleotide divergence, and for Hypsiglena we identified 79 toxin sequences that were grouped into 33 clusters. Comparisons of the venoms revealed divergent venom types, with Hypsiglena possessing a viper-like venom dominated by metalloproteinases, and B. irregularis having a more elapid-like venom, consisting primarily of three-finger toxins. CONCLUSIONS: Despite the difficulty of procuring venom from rear-fanged species, we were able to complete all analyses from a single specimen of each species without pooling venom samples or glands, demonstrating the power of high-definition transcriptomic and proteomic approaches. We found a high level of divergence in the venom types of two colubrids. These two venoms reflected the hemorrhagic/neurotoxic venom dichotomy that broadly characterizes the difference in venom strategies between elapids and viperids.
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spelling pubmed-42892262015-01-11 RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes McGivern, James J Wray, Kenneth P Margres, Mark J Couch, Michelle E Mackessy, Stephen P Rokyta, Darin R BMC Genomics Research Article BACKGROUND: Largely because of their direct, negative impacts on human health, the venoms of front-fanged snakes of the families Viperidae and Elapidae have been extensively characterized proteomically, transcriptomically, and pharmacologically. However, relatively little is known about the molecular complexity and evolution of the venoms of rear-fanged colubrid snakes, which are, with a few notable exceptions, regarded as harmless to humans. Many of these snakes have venoms with major effects on their preferred prey, and their venoms are probably as critical to their survival as those of front-fanged elapids and viperids. RESULTS: We sequenced the venom-gland transcriptomes from a specimen of Hypsiglena (Desert Night Snake; family Colubridae, subfamily Dipsadinae) and of Boiga irregularis (Brown Treesnake; family Colubridae, subfamily Colubrinae) and verified the transcriptomic results proteomically by means of high-definition mass spectrometry. We identified nearly 3,000 nontoxin genes for each species. For B. irregularis, we found 108 putative toxin transcripts in 46 clusters with <1% nucleotide divergence, and for Hypsiglena we identified 79 toxin sequences that were grouped into 33 clusters. Comparisons of the venoms revealed divergent venom types, with Hypsiglena possessing a viper-like venom dominated by metalloproteinases, and B. irregularis having a more elapid-like venom, consisting primarily of three-finger toxins. CONCLUSIONS: Despite the difficulty of procuring venom from rear-fanged species, we were able to complete all analyses from a single specimen of each species without pooling venom samples or glands, demonstrating the power of high-definition transcriptomic and proteomic approaches. We found a high level of divergence in the venom types of two colubrids. These two venoms reflected the hemorrhagic/neurotoxic venom dichotomy that broadly characterizes the difference in venom strategies between elapids and viperids. BioMed Central 2014-12-03 /pmc/articles/PMC4289226/ /pubmed/25476704 http://dx.doi.org/10.1186/1471-2164-15-1061 Text en © McGivern et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.
spellingShingle Research Article
McGivern, James J
Wray, Kenneth P
Margres, Mark J
Couch, Michelle E
Mackessy, Stephen P
Rokyta, Darin R
RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
title RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
title_full RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
title_fullStr RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
title_full_unstemmed RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
title_short RNA-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
title_sort rna-seq and high-definition mass spectrometry reveal the complex and divergent venoms of two rear-fanged colubrid snakes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4289226/
https://www.ncbi.nlm.nih.gov/pubmed/25476704
http://dx.doi.org/10.1186/1471-2164-15-1061
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