Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes)

Abstract

A 70-mer oligonucleotide-based microarray (1152 features) that emphasizes stress and immune responses factors was constructed to study transcriptomic responses of the snail Biomphalaria glabrata to different immune challenges. In addition to sequences with relevant putative ID and Gene Ontology (GO) annotation, the array features non-immune factors and unknown B. glabrata ESTs for functional gene discovery. The transcription profiles of B. glabrata (3 biological replicates, each a pool of 5 snails) were recorded at 12 hours post wounding, exposure to Gram negative or Gram positive bacteria (Escherichia coli and Micrococcus luteus, respectively), or infection with compatible trematode parasites (S. mansoni or E. paraensei, 20 miracidia/snail), relative to controls, using universal reference RNA. The data were subjected to Significance Analysis for Microarrays (SAM), with a false positive rate (FPR) ≤10%. Wounding yielded a modest differential expression profile (27 up/21 down) with affected features mostly dissimilar from other treatments. Partially overlapping, yet distinct expression profiles were recorded from snails challenged with E. coli (83 up/20 down) or M. luteus (120 up/42 down), mostly showing up-regulation of defense and stressrelated features. Significantly altered expression of selected immune features indicates that B. glabrata detects and responds differently to compatible trematodes. Echinostoma paraensei infection was associated mostly with down regulation of many (immune-) transcripts (42 up/68 down), whereas S. mansoni exposure yielded a preponderance of up-regulated features (140 up/23 down), with only few known immune genes affected. These observations may reflect the divergent strategies developed by trematodes during their evolution as specialized pathogens of snails to negate host

Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection

“…Because α-D-mannose was not bound by FREP3 in this study, it is likely the phagocytosis induced by α-Dmannose was because it was bound by mannose binding lectin, which has been identified in other invertebrates (30) and has been shown to be involved in the recognition and phagocytosis of pathogens (31,32). A C-type lectin-like sequence from B. glabrata with significant similarity to macrophage mannose receptor (20), The five large circles (diameter indicating frequency of recovery) represent the presumptive FREP3 source sequences. Note that the five snails had mostly the same source sequences.…”

“…A number of other phagocytosis-related transcripts were also shown to be up-regulated in resistant snails by our transcriptional analysis, underscoring the importance of this process in resistance to digenean infection (Table S1). Of particular interest is feature BGC0426, which, because of sequence similarities to dermatopontin (an extracellular matrix protein) and hemagglutinin/amebocyte aggregation factor (20), may attract hemocytes and regulate cellular adherence (Fig. 1A).…”

“…gnl|ti|2278068446-2278071234). pronounced during the early stages of infection (20): The parasite attempts to suppress the snail immune response (21) or to disguise itself from it (22), thereby allowing the parasite to establish. For its part, the snail host mounts humoral and cellular responses to encapsulate and kill the parasite (20,23,24).…”

“…pronounced during the early stages of infection (20): The parasite attempts to suppress the snail immune response (21) or to disguise itself from it (22), thereby allowing the parasite to establish. For its part, the snail host mounts humoral and cellular responses to encapsulate and kill the parasite (20,23,24). In some snaildigenean combinations, the snail is resistant to infection and the immune components responsible have been a frequent topic of study (23), in part because of the ramifications for interrupting transmission of schistosomes to humans.…”

Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei

“…This late suppression is in accordance with that observed in the present model of long term exposure to the myxosporean. Transcriptional studies have also demonstrated this gene suppression effect in other species, as in molluscs infected by the metazoan parasite Echinostoma paraensei, which had many down-regulated transcripts with potential immune functions (Adema et al, 2010), or in oysters chronically infected by the protozoan parasite Perkinus marinus (Wang et al, 2010).…”