A New Assessment of Thioester-Containing Proteins Diversity of the Freshwater Snail Biomphalaria glabrata

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.

iTRAQ‐based quantitative proteomic analysis in liver of Pomacea canaliculata induced by oleanolic acid stress

“…The C1q molecule found in invertebrates can act as a PRR, recognize multiple PAMPs, and participate in innate immune response 21 . A recent study also confirmed that macroglobulin plays an innate immunity role in mollusks 22 . In this study, the structures of the chitin‐binding protein, C1q protein domain, and A2M protein domain changed significantly under OA stress, which may indicate that P. canaliculata can resist OA stress through multiple mechanisms of immune response.…”

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

“…Faced with a wide variety of pathogens, the diversification of immune molecules appears to be the evolutionary path considered in invertebrates to mount a specific and effective defense response ( 99 , 124 – 126 ). In Biomphalaria , some large repertoires of genes that encode immune receptors such as FREPs, Toll-like receptor (TLR) or TEPs have been reported with more than 30, 50 or 11 genes respectively ( 46 , 63 , 99 , 127 ), while the number of effector genes identified may appear more restricted ( 128 ).…”

“…Some molecules of this proto-complement have been characterized from several mollusk species like Complement factor C2/B from Bivalvia such as Ruditapes decussates ( 147 ) or Sinonovacula constricta ( 148 ), C3-like factors from mussels ( 149 ) or clams ( 150 ), but few studies led to the characterization of the whole system ( 145 , 151 ). While a diversity of C3-like proteins within the TEP superfamily has been reported ( 63 , 99 ) as well as a large repertoire of carbohydrate-binding proteins such as FREPs ( 46 , 152 ) and VIgL domain-containing proteins in B. glabrata ( 53 , 112 ), no complement factor C2/B-like protein has yet been identified. As the small lobe from several biomphalysins is structurally close to the CCP domain of Factor B, we speculated that biomphalysins could be involved in the activation of the proto-complement system by binding with TEPs.…”

“…DNase treatment and reverse transcription of RNA (4µg) into cDNA were performed with Maxima H minus first strand cDNA synthesis kit (ThermoFisher Scientific, Waltham, MA, USA) using random hexamer according to the manufacturer’s instructions. Real-time RT-PCR analyses were performed using the LightCycler 480 System (Roche) performed in the same way as described in ( 63 ). Only primer couples ( Table S2 ) with amplification efficiency of 2 were retained.…”

Hemocyte siRNA uptake is increased by 5′ cholesterol-TEG addition in Biomphalaria glabrata, snail vector of schistosome

“…The first is functional redundancy between members of the same multigene family. Recently, it was highlighted that BgTEP1 belongs to a multigenic family harboring at least ten other members comprising three C3-like complement factors, one alpha-2-macroglobulin, two macroglobulin complement-related proteins, four insect-like TEP including BgTEP1 and one CD109 molecule ( Castillo et al, 2020 ; Duval et al, 2020 ). In many invertebrate organisms, several genes encoding TEPs have been identified, fifteen from Anopheles gambiae , six from Drosophila melanogaster or nine from the tick Ixodes ricinus genomes, to name a few examples.…”