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(Referência obtida automaticamente do Web of Science, por meio da informação sobre o financiamento pela FAPESP e o número do processo correspondente, incluída na publicação pelos autores.)

Replacement and Parallel Simplification of Nonhomologous Proteinases Maintain Venom Phenotypes in Rear-Fanged Snakes

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Autor(es):
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Bayona-Serrano, Juan David [1] ; Viala, Vincent Louis [1, 2] ; Rautsaw, Rhett M. [3] ; Schramer, Tristan D. [3] ; Barros-Carvalho, Gesiele A. [1] ; Nishiyama, Jr., Milton Yutaka [1, 2] ; Freitas-de-Sousa, Luciana A. [4] ; Moura-da-Silva, Ana Maria [4, 5] ; Parkinson, Christopher L. [3, 6] ; Grazziotin, Felipe Gobbi [7] ; Junqueira-de-Azevedo, Inacio L. M. [1, 2]
Número total de Autores: 11
Afiliação do(s) autor(es):
[1] Inst Butantan, Lab Especial Toxinol Aplicada, Sao Paulo - Brazil
[2] Ctr Toxins Immune Response & Cell Signaling CeTIC, Sao Paulo - Brazil
[3] Clemson Univ, Dept Biol Sci, Clemson, SC 29634 - USA
[4] Inst Butantan, Lab Imunopatol, Sao Paulo - Brazil
[5] Inst Pesquisa Clin Carlos Borborema, Fundacao Med Trop Dr Heitor Vieira Dourado, Manaus, Amazonas - Brazil
[6] Clemson Univ, Dept Forestry & Environm Conservat, Clemson, SC - USA
[7] Inst Butantan, Lab Colecoes Zool, Sao Paulo - Brazil
Número total de Afiliações: 7
Tipo de documento: Artigo Científico
Fonte: Molecular Biology and Evolution; v. 37, n. 12, p. 3563-3575, DEC 2020.
Citações Web of Science: 1
Resumo

Novel phenotypes are commonly associated with gene duplications and neofunctionalization, less documented are the cases of phenotypic maintenance through the recruitment of novel genes. Proteolysis is the primary toxic character of many snake venoms, and ADAM metalloproteinases, named snake venom metalloproteinases (SVMPs), are largely recognized as the major effectors of this phenotype. However, by investigating original transcriptomes from 58 species of advanced snakes (Caenophidia) across their phylogeny, we discovered that a different enzyme, matrix metalloproteinase (MMP), is actually the dominant venom component in three tribes (Tachymenini, Xenodontini, and Conophiini) of rear-fanged snakes (Dipsadidae). Proteomic and functional analyses of these venoms further indicate that MMPs are likely playing an ``SVMP-like{''} function in the proteolytic phenotype. A detailed look into the venom-specific sequences revealed a new highly expressed MMP subtype, named snake venom MMP (svMMP), which originated independently on at least three occasions from an endogenous MMP-9. We further show that by losing ancillary noncatalytic domains present in its ancestors, svMMPs followed an evolutionary path toward a simplified structure during their expansion in the genomes, thus paralleling what has been proposed for the evolution of their Viperidae counterparts, the SVMPs. Moreover, we inferred an inverse relationship between the expression of svMMPs and SVMPs along the evolutionary history of Xenodontinae, pointing out that one type of enzyme may be substituting for the other, whereas the general (metallo)proteolytic phenotype is maintained. These results provide rare evidence on how relevant phenotypic traits can be optimized via natural selection on nonhomologous genes, yielding alternate biochemical components. (AU)

Processo FAPESP: 17/24498-9 - Análises venômicas de serpentes Dipsadidae focando em adaptações a ofiofagia
Beneficiário:Juan David Bayona Serrano
Linha de fomento: Bolsas no Brasil - Doutorado Direto
Processo FAPESP: 16/50127-5 - Dimensions US-BIOTA São Paulo: scales of biodiversity: integrated studies of snake venom evolution and function across multiple levels of diversity
Beneficiário:Inácio de Loiola Meirelles Junqueira de Azevedo
Linha de fomento: Auxílio à Pesquisa - Programa BIOTA - Temático
Processo FAPESP: 13/07467-1 - CeTICS - Centro de Toxinas, Imuno-Resposta e Sinalização Celular
Beneficiário:Hugo Aguirre Armelin
Linha de fomento: Auxílio à Pesquisa - Centros de Pesquisa, Inovação e Difusão - CEPIDs
Processo FAPESP: 17/24546-3 - Escalas da biodiversidade: estudos integrados da evolução de serpentes e função do veneno
Beneficiário:Luciana Aparecida Freitas de Sousa
Linha de fomento: Bolsas no Brasil - Pós-Doutorado