New Insights Into Biomphalysin Gene Family Diversification in the Vector Snail Biomphalaria glabrata

Type Article
Date 2021-04
Language English
Author(s) Pinaud Silvain1, 2, Tetreau Guillaume1, 2, Poteaux Pierre1, 2, Galinier Richard1, 2, Chaparro Cristian1, 2, Lassalle Damien1, 2, Portet Anaïs1, 2, Simphor Elodie1, 2, Gourbal Benjamin1, 2, Duval David1, 2
Affiliation(s) 1 : IHPE, Univ Montpellier, CNRS, IFREMER, Univ Perpignan Via Domitia, Perpignan, France
2 : CNRS, IFREMER, University of Montpellier, Perpignan, France
Source Frontiers In Immunology (1664-3224) (Frontiers Media SA), 2021-04 , Vol. 12 , P. 635131 (19p.)
DOI 10.3389/fimmu.2021.635131
WOS© Times Cited 11
Keyword(s) biomphalaria, biomphalysin, aerolysin, invertebrate immunity, pore-forming toxin (PFT), structure

Aerolysins initially characterized as virulence factors in bacteria are increasingly found in massive genome and transcriptome sequencing data from metazoans. Horizontal gene transfer has been demonstrated as the main way of aerolysin-related toxins acquisition in metazoans. However, only few studies have focused on their potential biological functions in such organisms. Herein, we present an extensive characterization of a multigene family encoding aerolysins - named biomphalysin - in Biomphalaria glabrata snail, the intermediate host of the trematode Schistosoma mansoni. Our results highlight that duplication and domestication of an acquired bacterial toxin gene in the snail genome result in the acquisition of a novel and diversified toxin family. Twenty-three biomphalysin genes were identified. All are expressed and exhibited a tissue-specific expression pattern. An in silico structural analysis was performed to highlight the central role played by two distinct domains i) a large lobe involved in the lytic function of these snail toxins which constrained their evolution and ii) a small lobe which is structurally variable between biomphalysin toxins and that matched to various functional domains involved in moiety recognition of targets cells. A functional approach suggests that the repertoire of biomphalysins that bind to pathogens, depends on the type of pathogen encountered. These results underline a neo-and sub-functionalization of the biomphalysin toxins, which have the potential to increase the range of effectors in the snail’s immune arsenal.

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Supplementary Figure 1 | Dot plot of the different biomphalysins and their surrounding genomic regions. The first row and column ... 1 283 KB Open access
Supplementary Figure 2 | Sequence alignment and predicted topology of biomphalysin proteins. Multiple alignment of the biomphalysin proteins was performed using CLUSTALO. 3 451 KB Open access
Supplementary Figure 3 | TMD characterization in biomphalysin proteins. (A) Multiple alignment of the region surrounding the transmembrane domain of all biomphalysin proteins was performed ... 1 234 KB Open access
Supplementary Figure 4 | Carbohydrate binding site prediction on biomphalysin proteins. (A) Surface representation of biomphalysin16 protein interacting with alpha-D mannose-6-phosphate (PDB: M6P). 14 MB Open access
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Pinaud Silvain, Tetreau Guillaume, Poteaux Pierre, Galinier Richard, Chaparro Cristian, Lassalle Damien, Portet Anaïs, Simphor Elodie, Gourbal Benjamin, Duval David (2021). New Insights Into Biomphalysin Gene Family Diversification in the Vector Snail Biomphalaria glabrata. Frontiers In Immunology, 12, 635131 (19p.). Publisher's official version : , Open Access version :