Changes in the neuropeptide content of Biomphalaria ganglia nervous system following Schistosoma infection

Abstract

BackgroundMolluscs, including snails, are prone to parasite infection, which can lead to massive physiological and behavioural changes, yet many of the molecular components involved remain unresolved. Central to this point is the neural system that in snails consists of several ganglia that regulate the animals’ physiology and behaviour patterns. The availability of a genomic resource for the freshwater snail Biomphalaria glabrata provides a mean towards the high throughput analysis of changes in the central nervous system (CNS) following infection with Schistosoma miracidia.ResultsIn this study, we performed a proteomic analysis of the B. glabrata CNS at pre-patent infection, providing a list of proteins that were further used within a protein-protein interaction (PPI) framework against S. mansoni proteins. A hub with most connections for both non-infected and infected Biomphalaria includes leucine aminopeptidase 2 (LAP2), which interacts with numerous miracidia proteins that together belong to the immunoglobulin family of cell adhesion related molecules. We additionally reveal the presence of at least 165 neuropeptides derived from the precursors of buccalin, enterin, FMRF, FVRI, pedal peptide 1, 2, 3 and 4, RYamide, RFamide, pleurin and others. Many of these were present at significantly reduced levels in the snail’s CNS post-infection, such as the egg laying hormone, a neuropeptide required to initiate egg laying in gastropod molluscs.ConclusionsOur analysis demonstrates that LAP2 may be a key component that regulates parasite infection physiology, as well as establishing that parasite-induced reproductive castration may be facilitated by significant reductions in reproduction-associated neuropeptides. This work helps in our understanding of molluscan neuropeptides and further stimulates advances in parasite-host interactions.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2218-1) contains supplementary material, which is available to authorized users.

Striking differences in virulence, transmission and sporocyst growth dynamics between two schistosome populations

“…Schistosome parasites have a direct impact on their snail intermediate hosts; as they grow and generate cercariae, sporocysts deplete galactogen in the albumen gland and consume the ovotestis and hepatopancreas, converting stored glycogen to glucose [11, 12]. Wang et al [40] found that neuropeptides and precursor proteins involved in snail reproduction were heavily downregulated in infected prepatent snails compared to uninfected snails, suggesting that this could play a role in castration of Biomphalaria snails by schistosomes. Other downregulated neuropeptides in prepatent snails were linked to snail feeding and growth, process that directly impact the reproductive capacity, metabolism and immunity of the snail host.…”

Striking differences in virulence, transmission, and sporocyst growth dynamics between two schistosome populations

“…Schistosome parasites have a direct impact on their snail intermediate hosts: as they grow and generate cercariae, sporocysts deplete galactogen in the albumen gland and consume the ovotestis and hepatopancreas, converting stored glycogen to glucose [10,35]. Wang and colleagues [36] found that neuropeptides and precursor proteins involved in snail reproduction were heavily down regulated in infected prepatent snails compared to uninfected snails, suggesting that this could play a role in castration of Biomphalaria snails by schistosomes. Other down regulated neuropeptides in prepatent snails were linked to snail feeding and growth, process that directly impact the reproductive capacity, metabolism and immunity of the snail host.…”

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

“…Myomodulins are neurotransmitters involved in regulating feeding behavior by controlling radula protractor muscles used for feeding [62] in Lymnaea stagnalis [63] and Aplysia californica [64]. Myomodulin is down-regulated in prepatent S. mansoni-infected B. glabrata and this was implicated as possibly diminishing feeding efficiency in infected snails [65]. Down-regulation of a B. pfeifferi feeding circuitry peptide was seen in early and patent S. mansoni infections [23].…”