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J Proteomics. 2018 Jun 15;181:60-72. doi: 10.1016/j.jprot.2018.03.032. Epub 2018 Apr 3.

Molecular mechanisms underlying intraspecific variation in snake venom.

Author information

1
Laboratório de Imunopatologia, Instituto Butantan, Av. Vital Brazil, 1500, 05503-900 São Paulo, SP, Brazil.
2
Laboratório Especial de Toxinologia Aplicada, Instituto Butantan, Av. Vital Brazil, 1500, 05503-900 São Paulo, SP, Brazil.
3
Laboratório de Toxinologia, Instituto Oswaldo Cruz - IOC/FIOCRUZ, Av. Brasil, 4365, 21040-900 Rio de Janeiro, RJ, Brazil.
4
Programa de Pós-Graduação em Recursos Naturais da Amazônia, Laboratório de Bioprospecção e Biologia Experimental, Universidade Federal do Oeste do Pará - UFOPA, Rua Vera Paz, s/n, 68035-110 Santarém, PA, Brazil.
5
Faculdades Integradas do Tapajós/Faculdade da Amazônia - FIT/UNAMA, Rua Rosa Vermelha, 335, 68010-200 Santarém, PA, Brazil.
6
Laboratório Especial de Coleções Zoológicas, Instituto Butantan, Av. Vital Brazil, 1500, 05503-900 São Paulo, SP, Brazil.
7
Department of Biological Science, Florida State University, Tallahassee, FL 32306, USA.
8
Department of Evolution, Ecology and Organismal Biology Ohio State University, Columbus, OH 43210, USA.
9
Laboratório Especial de Toxinologia Aplicada, Instituto Butantan, Av. Vital Brazil, 1500, 05503-900 São Paulo, SP, Brazil. Electronic address: inacio.azevedo@butantan.gov.br.
10
Laboratório de Imunopatologia, Instituto Butantan, Av. Vital Brazil, 1500, 05503-900 São Paulo, SP, Brazil. Electronic address: ana.moura@butantan.gov.br.

Abstract

Elucidating the molecular mechanisms underlying snake venom variability provides important clues for understanding how the biological functions of this powerful toxic arsenal evolve. We analyzed in detail individual transcripts and venom protein isoforms produced by five specimens of a venomous snake (Bothrops atrox) from two nearby but genetically distinct populations from the Brazilian Amazon rainforest which show functional similarities in venom properties. Individual variation was observed among the venoms of these specimens, but the overall abundance of each general toxin family was conserved both in transcript and in venom protein levels. However, when expression of independent paralogues was analyzed, remarkable differences were observed within and among each toxin group, both between individuals and between populations. Transcripts for functionally essential venom proteins ("core function" proteins) were highly expressed in all specimens and showed similar transcription/translation rates. In contrast, other paralogues ("adaptive" proteins) showed lower expression levels and the toxins they coded for varied among different individuals. These results provide support for the inferences that (a) expression and translational differences play a greater role in defining adaptive variation in venom phenotypes than does sequence variation in protein coding genes and (b) convergent adaptive venom phenotypes can be generated through different molecular mechanisms.

SIGNIFICANCE:

Analysis of individual transcripts and venom protein isoforms produced by specimens of a venomous snake (Bothrops atrox), from the Brazilian Amazon rainforest, revealed that transcriptional and translational mechanisms contribute to venom phenotypic variation. Our finding of evidence for high expression of toxin proteins with conserved function supports the hypothesis that the venom phenotype consists of two kinds of proteins: conserved "core function" proteins that provide essential functional activities with broader relevance and less conserved "adaptive" proteins that vary in expression and may permit customization of protein function. These observations allowed us to suggest that genetic mechanisms controlling venom variability are not restricted to selection of gene copies or mutations in structural genes but also to selection of the mechanisms controlling gene expression, contributing to the plasticity of this important phenotype for venomous snakes.

KEYWORDS:

Evolution; Plasticity; Proteome; Snake venom; Toxin function; Transcriptome

PMID:
29621647
DOI:
10.1016/j.jprot.2018.03.032
[Indexed for MEDLINE]

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