The Venom Composition of the Snake Tribe Philodryadini: ‘Omic’ Techniques Reveal Intergeneric Variability among South American Racers

Author:

Tioyama Emilly Campos12ORCID,Bayona-Serrano Juan David13,Portes-Junior José A.2,Nachtigall Pedro Gabriel3ORCID,de Souza Vinicius Carius3,Beraldo-Neto Emidio4ORCID,Grazziotin Felipe Gobbi5ORCID,Junqueira-de-Azevedo Inácio L. M.3,Moura-da-Silva Ana Maria2ORCID,Freitas-de-Sousa Luciana Aparecida2

Affiliation:

1. Programa de Pós-Graduação em Ciências-Toxinologia, Escola Superior do Instituto Butantan, São Paulo 05508-210, Brazil

2. Laboratório de Imunopatologia, Instituto Butantan, São Paulo 05503-900, Brazil

3. Laboratório de Toxinologia Aplicada, Instituto Butantan, São Paulo 05503-900, Brazil

4. Laboratório de Bioquímica e Biofísica, Instituto Butantan, São Paulo 05503-900, Brazil

5. Laboratório de Coleções Zoológicas, Instituto Butantan, São Paulo 05503-900, Brazil

Abstract

Snakes of the Philodryadini tribe are included in the Dipsadidae family, which is a diverse group of rear-fanged snakes widespread in different ecological conditions, including habitats and diet. However, little is known about the composition and effects of their venoms despite their relevance for understanding the evolution of these snakes or even their impact on the occasional cases of human envenoming. In this study, we integrated venom gland transcriptomics, venom proteomics and functional assays to characterize the venoms from eight species of the Philodryadini tribe, which includes the genus Philodryas, Chlorosoma and Xenoxybelis. The most abundant components identified in the venoms were snake venom metalloproteinases (SVMPs), cysteine-rich secretory proteins (CRISPs), C-type lectins (CTLs), snake endogenous matrix metalloproteinases type 9 (seMMP-9) and snake venom serinoproteinases (SVSPs). These protein families showed a variable expression profile in each genus. SVMPs were the most abundant components in Philodryas, while seMMP-9 and CRISPs were the most expressed in Chlorosoma and Xenoxybelis, respectively. Lineage-specific differences in venom composition were also observed among Philodryas species, whereas P. olfersii presented the highest amount of SVSPs and P. agassizii was the only species to express significant amounts of 3FTx. The variability observed in venom composition was confirmed by the venom functional assays. Philodryas species presented the highest SVMP activity, whereas Chlorosoma species showed higher levels of gelatin activity, which may correlate to the seMMP-9 enzymes. The variability observed in the composition of these venoms may be related to the tribe phylogeny and influenced by their diets. In the presented study, we expanded the set of venomics studies of the Philodryadini tribe, which paves new roads for further studies on the evolution and ecology of Dipsadidae snakes.

Funder

São Paulo Research Foundation

Coordenação de Aperfeicoamento de Pessoal de Nível Superior

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Publisher

MDPI AG

Subject

Health, Toxicology and Mutagenesis,Toxicology

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