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Abstract
BackgroundThe AIG (avrRpt2-induced gene) family of GTPases, characterized by the presence of a distinctive AIG1 domain, is mysterious in having a peculiar phylogenetic distribution, a predilection for undergoing expansion and loss, and an uncertain functional role, especially in invertebrates. AIGs are frequently represented as GIMAPs (GTPase of the immunity associated protein family), characterized by presence of the AIG1 domain along with coiled-coil domains. Here we provide an overview of the remarkably expanded AIG repertoire of the freshwater gastropod Biomphalaria glabrata, compare it with AIGs in other organisms, and detail patterns of expression in B. glabrata susceptible or resistant to infection with Schistosoma mansoni, responsible for the neglected tropical disease of intestinal schistosomiasis.ResultsWe define the 7 conserved motifs that comprise the AIG1 domain in B. glabrata and detail its association with at least 7 other domains, indicative of functional versatility of B. glabrata AIGs. AIG genes were usually found in tandem arrays in the B. glabrata genome, suggestive of an origin by segmental gene duplication. We found 91 genes with complete AIG1 domains, including 64 GIMAPs and 27 AIG genes without coiled-coils, more than known for any other organism except Danio (with > 100). We defined expression patterns of AIG genes in 12 different B. glabrata organs and characterized whole-body AIG responses to microbial PAMPs, and of schistosome-resistant or -susceptible strains of B. glabrata to S. mansoni exposure. Biomphalaria glabrata AIG genes clustered with expansions of AIG genes from other heterobranch gastropods yet showed unique lineage-specific subclusters. Other gastropods and bivalves had separate but also diverse expansions of AIG genes, whereas cephalopods seem to lack AIG genes.ConclusionsThe AIG genes of B. glabrata exhibit expansion in both numbers and potential functions, differ markedly in expression between strains varying in susceptibility to schistosomes, and are responsive to immune challenge. These features provide strong impetus to further explore the functional role of AIG genes in the defense responses of B. glabrata, including to suppress or support the development of medically relevant S. mansoni parasites.
Highlights
The AIG family of GTPases, characterized by the presence of a distinctive AvrRpt2-induced gene (AIG1) domain, is mysterious in having a peculiar phylogenetic distribution, a predilection for undergoing expansion and loss, and an uncertain functional role, especially in invertebrates
The following definitions are used throughout the paper: AIG1 domain: a conserved domain including G1-G4, G5/Immune-associated nucleotide-binding proteins (IAN) motifs and a conserved box (CB) found with the predicted protein sequences; partial AIG gene: gene containing an incomplete AIG1 domain, with absence of at least one conserved motif; AIG gene: gene containing at least one complete AIG1 domain, and possibly other domains; B. glabrata GTPases of immunity associated proteins (GIMAP): B. glabrata gene containing a complete AIG1 domain and one or more coiledcoil domains
Conserved motifs within the B. glabrata AIG1 domain Conserved motifs (G1-G4, G5/IAN and CB) within the AIG1 domains of B. glabrata are indicated in Fig. 1, with more details in Additional file 2: Table S1, and occur in the order expected
Summary
The AIG (avrRpt2-induced gene) family of GTPases, characterized by the presence of a distinctive AIG1 domain, is mysterious in having a peculiar phylogenetic distribution, a predilection for undergoing expansion and loss, and an uncertain functional role, especially in invertebrates. AIGs are frequently represented as GIMAPs (GTPase of the immunity associated protein family), characterized by presence of the AIG1 domain along with coiled-coil domains. One example of a group of immune-related molecules first discovered in plants and mammals is the AIG family of GTPases. The AIG family of GTPases is frequently represented by GIMAPs (GTPase of the immunity associated protein family), known as immune-associated nucleotide binding proteins or IANs. GIMAPs are proteins of 30–80 kDa containing coiled-coil regions along with a characteristic AIG1 domain. Some GIMAP genes encode proteins with membrane-anchoring domains whereas others are soluble proteins [16]
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