Abstract
Thioester-containing proteins (TEPs) superfamily is known to play important innate immune functions in a wide range of animal phyla. TEPs are involved in recognition, and in the direct or mediated killing of several invading organisms or pathogens. While several TEPs have been identified in many invertebrates, only one TEP (named BgTEP) has been previously characterized in the freshwater snail, Biomphalaria glabrata. As the presence of a single member of that family is particularly intriguing, transcriptomic data and the recently published genome were used to explore the presence of other BgTEP related genes in B. glabrata. Ten other TEP members have been reported and classified into different subfamilies: Three complement-like factors (BgC3-1 to BgC3-3), one α-2-macroblobulin (BgA2M), two macroglobulin complement-related proteins (BgMCR1, BgMCR2), one CD109 (BgCD109), and three insect TEP (BgTEP2 to BgTEP4) in addition to the previously characterized BgTEP that we renamed BgTEP1. This is the first report on such a level of TEP diversity and of the presence of macroglobulin complement-related proteins (MCR) in mollusks. Gene structure analysis revealed alternative splicing in the highly variable region of three members (BgA2M, BgCD109, and BgTEP2) with a particularly unexpected diversity for BgTEP2. Finally, different gene expression profiles tend to indicate specific functions for such novel family members.
Highlights
Thioester-containing proteins (TEP) are large secreted proteins playing central roles in the innate immune response [1,2]
(BgTEPs) identified with various orthologous sequences recovered from other animal species, a identified with various orthologous sequences recovered from other animal species, a phylogenetic phylogenetic analysis was performed using 123 other sequences (Table S2)
Particular attention was paid to BgTEP2 gene for which we identified 12 possible variants from to BgTEP2 gene for which we identified 12 possible variants from B. glabrata transcriptomes (Figure 3C, B. glabrata transcriptomes (Figure 3C, Table S3), of which only one was predicted from BglaB1
Summary
Thioester-containing proteins (TEP) are large secreted proteins playing central roles in the innate immune response [1,2]. ITEP was only found for Protostomia, MCR was, until now, only reported for arthropods, whereas complement factor TEP was never found in available insect genomes while present in all other arthropod groups. Several studies have investigated key molecules of snail immune system and parasite virulence factors in order to decipher the molecular dialogue between B. glabrata and S. mansoni, and to explain this compatibility polymorphism phenotype [30,38,39,40,41,42,43]. A recent study characterized this BgTEP as being similar to insect TEP, secreted by hemocytes, expressed following immune challenges, and able to bind to different pathogen teguments including the parasite S. mansoni [45]. We determined the tissue expression pattern of BgTEP genes by quantitative PCR
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