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Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni.

ABSTRACT: Biomphalaria glabrata (B. glabrata) is an air-breathing aquatic mollusc found in freshwater habitats across the Western Hemisphere. It is most well-known for its recognized capacity to act as a major intermediate host for Schistosoma mansoni, the human blood fluke parasite. Ionotropic receptors (IRs), a variant family of the ionotropic glutamate receptors (iGluR), have an evolutionary ancient function in detecting odors to initiate chemosensory signaling. In this study, we applied an array of methods towards the goal of identifying IR-like family members in B. glabrata, ultimately revealing two types, the iGluR and IR. Sequence alignment showed that three ligand-binding residues are conserved in most Biomphalaria iGluR sequences, while the IRs did exhibit a variable pattern, lacking some or all known glutamate-interactingresidues, supporting their distinct classification from the iGluRs. We show that B. glabrata contains 7 putative IRs, some of which are expressed within its chemosensory organs. To further investigate a role for the more ancient IR25a type in chemoreception, we tested its spatial distribution pattern within the snail cephalic tentacle by in situ hybridization. The presence of IR25a within presumptive sensory neurons supports a role for this receptor in olfactory processing, contributing to our understanding of the molecular pathways that are involved in Biomphalaria olfactory processing.

SUBMITTER: Liang D

PROVIDER: S-EPMC4890853 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni.

Liang Di D Wang Tianfang T Rotgans Bronwyn A BA McManus Donald P DP Cummins Scott F SF

PloS one 20160602 6

Biomphalaria glabrata (B. glabrata) is an air-breathing aquatic mollusc found in freshwater habitats across the Western Hemisphere. It is most well-known for its recognized capacity to act as a major intermediate host for Schistosoma mansoni, the human blood fluke parasite. Ionotropic receptors (IRs), a variant family of the ionotropic glutamate receptors (iGluR), have an evolutionary ancient function in detecting odors to initiate chemosensory signaling. In this study, we applied an array of me ...[more]

PMID: 27253696

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Project description:Biomphalaria glabrata is the mollusc intermediate host for Schistosoma mansoni, a digenean flatworm parasite that causes human intestinal schistosomiasis. An estimated 200 million people in 74 countries suffer from schistosomiasis, in terms of morbidity this is the most severe tropical disease after malaria. Epigenetic information informs on the status of gene activity that is heritable, for which changes are reversible and that is not based on the DNA sequence. Epigenetic mechanisms generate variability that provides a source for potentially heritable phenotypic variation and therefore could be involved in the adaptation to environmental constraint. Phenotypic variations are particularly important in host-parasite interactions in which both selective pressure and rate of evolution are high. In this context, epigenetic changes are expected to be major drivers of phenotypic plasticity and co-adaptation between host and parasite. Consequently, with characterization of the genomes of invertebrates that are parasite vectors or intermediate hosts, it is also essential to understand how the epigenetic machinery functions to better decipher the interplay between host and parasite.The CpGo/e ratios were used as a proxy to investigate the occurrence of CpG methylation in B. glabrata coding regions. The presence of DNA methylation in B. glabrata was also confirmed by several experimental approaches: restriction enzymatic digestion with isoschizomers, bisulfite conversion based techniques and LC-MS/MS analysis.In this work, we report that DNA methylation, which is one of the carriers of epigenetic information, occurs in B. glabrata; approximately 2% of cytosine nucleotides are methylated. We describe the methylation machinery of B. glabrata. Methylation occurs predominantly at CpG sites, present at high ratios in coding regions of genes associated with housekeeping functions. We also demonstrate by bisulfite treatment that methylation occurs in multiple copies of Nimbus, a transposable element.This study details DNA methylation for the first time, one of the carriers of epigenetic information in B. glabrata. The general characteristics of DNA methylation that we observed in the B. glabrata genome conform to what epigenetic studies have reported from other invertebrate species.

Project description:BackgroundFreshwater snails are the intermediate hosts of a large variety of trematode flukes such as Schistosoma mansoni responsible for one of the most important parasitic diseases caused by helminths, affecting 67 million people worldwide. Recently, the WHO Global Vector Control Response 2017-2030 (GVCR) programme reinforced its message for safer molluscicides as part of required strategies to strengthen vector control worldwide. Here, we present the essential oil from Eryngium triquetrum as a powerful product with molluscicide and parasiticide effect against S. mansoni and the snail intermediate host Biomphalaria glabrata.MethodsIn the present study, we describe using several experimental approaches, the chemical composition of E. triquetrum essential oil extract and its biological effects against the snail B. glabrata and its parasite S. mansoni. Vector and the free-swimming larval stages of the parasite were exposed to different oil concentrations to determine the lethal concentration required to produce a mortality of 50% (LC50) and 90% (LC90). In addition, toxic activity of this essential oil was analyzed against embryos of B. glabrata snails by monitoring egg hatching and snail development. Also, short-time exposure to sublethal molluscicide concentrations on S. mansoni miracidia was performed to test a potential effect on parasite infectivity on snails. Mortality of miracidia and cercariae of S. mansoni is complete for 5, 1 and 0.5 ppm of oil extract after 1 and 4 h exposure.ResultsThe major chemical component found in E. triquetrum oil determined by GC-FID and GC/MS analyses is an aliphatic polyacetylene molecule, the falcarinol with 86.9-93.1% of the total composition. The LC50 and LC90 values for uninfected snails were 0.61 and 1.02 ppm respectively for 24 h exposure. At 0.5 ppm, the essential oil was two times more toxic to parasitized snails with a mortality rate of 88.8 ± 4.8%. Moderate embryonic lethal effects were observed at the concentration of 1 ppm. Severe surface damage in miracidia was observed with a general loss of cilia that probably cause their immobility. Miracidia exposed 30 min to low concentration of plant extract (0.1 ppm) were less infective with 3.3% of prevalence compare to untreated with a prevalence of 44%.ConclusionsEssential oil extracted from E. triquetrum and falcarinol must be considered as a promising product for the development of new interventions for schistosomiasis control and could proceed to be tested on Phase II according to the WHO requirements.

Dataset Information

Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni.

Publications

Ionotropic Receptors Identified within the Tentacle of the Freshwater Snail Biomphalaria glabrata, an Intermediate Host of Schistosoma mansoni.

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