Size Matters: An Evaluation of the Molecular Basis of Ontogenetic Modifications in the Composition of Bothrops jararacussu Snake Venom.

Luciana A Freitas-De-Sousa,Felipe G Grazziotin,Pedro G Nachtigall,Bruno R Silva,José A Portes-Junior,Tobias S Kunz,Schyler A Ellsworth,Flora Ortiz,Inácio L M Junqueira-De-Azevedo,Gunnar S Nystrom,Emilly Tioyama,Noranathan C Guimarães,Ana M Moura-Da-Silva,Darin R Rokyta,Matthew L Holding

doi:10.3390/toxins12120791

Luciana A Freitas-De-Sousa, Felipe G Grazziotin + Show 13 more

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https://doi.org/10.3390/toxins12120791

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Abstract

Ontogenetic changes in venom composition have been described in Bothrops snakes, but only a few studies have attempted to identify the targeted paralogues or the molecular mechanisms involved in modifications of gene expression during ontogeny. In this study, we decoded B. jararacussu venom gland transcripts from six specimens of varying sizes and analyzed the variability in the composition of independent venom proteomes from 19 individuals. We identified 125 distinct putative toxin transcripts, and of these, 73 were detected in venom proteomes and only 10 were involved in the ontogenetic changes. Ontogenetic variability was linearly related to snake size and did not correspond to the maturation of the reproductive stage. Changes in the transcriptome were highly predictive of changes in the venom proteome. The basic myotoxic phospholipases A2 (PLA2s) were the most abundant components in larger snakes, while in venoms from smaller snakes, PIII-class SVMPs were the major components. The snake venom metalloproteinases (SVMPs) identified corresponded to novel sequences and conferred higher pro-coagulant and hemorrhagic functions to the venom of small snakes. The mechanisms modulating venom variability are predominantly related to transcriptional events and may consist of an advantage of higher hematotoxicity and more efficient predatory function in the venom from small snakes.

Highlights

IntroductionAdvanced snakes (clade Caenophidia) have acquired the ability to produce, secrete, and inject venoms
Advanced snakes have acquired the ability to produce, secrete, and inject venoms
The variability in venom composition of B. jararacussu snakes was analyzed in this study using a group of nineteen snakes recently collected in São Paulo, Santa Catarina, and Rio de Janeiro states of Brazil (Supplementary Figure S1), including ten females and nine males with snout-vent lengths (SVL) ranging from 257 to 1230 mm (Supplementary Table S1)

Summary

Introduction

Advanced snakes (clade Caenophidia) have acquired the ability to produce, secrete, and inject venoms. Snake venoms are mainly composed of proteic toxins, the genes of which have been recruited early during Caenophidia diversification. These ancestor genes underwent duplications, and the copies recruited for venom were diversified through several genetic mechanisms resulting in neofunctionalization [1,2,3,4]. The differential expression of those distinct paralogues allows for a wide diversity of snake venom phenotypes and an astonishing variability observed across multiple taxonomic and intraspecific levels. The high degree of variability in venom composition is implicated as a key factor in the occupation of different ecological niches by the advanced snakes [1,5]

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