Thein vivotranscriptome ofSchistosoma mansoniin two prominent vector species,Biomphalaria pfeifferiandB. glabrata

Abstract

ABSTRACTBackgroundThe full scope of the genes expressed by schistosomes during intramolluscan development has yet to be characterized. Understanding the gene products deployed by larval schistosomes in their snail hosts will provide insights into their establishment, maintenance, asexual reproduction, ability to castrate their hosts, and their prolific production of human-infective cercariae. Using the Illumina platform, the intramolluscan transcriptome ofSchistosoma mansoniwas investigated in field-derived specimens of the prominent vector speciesBiomphalaria pfeifferiat 1 and 3 days post infection (d) and from snails shedding cercariae. TheseS. mansonisamples were derived from the same snails used in our complementaryB. pfeifferitranscriptomic study. We supplemented this view with microarray analyses ofS. mansonifromB. glabrataat 2d, 4d, 8d, 16d, and 32d.Principal FindingsTranscripts representing at least 7,740 (66%) of knownS. mansonigenes were expressed during intramolluscan development, with the greatest number expressed in snails shedding cercariae. Many transcripts were constitutively expressed throughout development featuring membrane transporters, and metabolic enzymes involved in protein and nucleic acid synthesis and cell division. Several proteases and protease inhibitors were expressed at all stages, including some proteases usually associated with cercariae. Transcripts associated with G-protein coupled receptors, germ cell perpetuation, and stress responses and defense were well represented. We noted transcripts homologous to planarian anti-bacterial factors, several neural development or neuropeptide transcripts including neuropeptide Y, and receptors that may be associated with schistosome germinal cell maintenance and that could also impact host reproduction. In at least one snail the presence of larvae of another digenean species (an amphistome) was associated with repressedS. mansonitranscriptional activity.Conclusions/SignificanceThisin vivostudy, particularly featuring field-derived snails and schistosomes, provides a distinct view from previous studies of development of cultured intramolluscan stages from lab-maintained organisms. We found many highly represented transcripts with suspected or unknown functions, with connection to intramolluscan development yet to be elucidated.AUTHOR SUMMARYSchistosoma mansoniis one of the most important schistosome species causing the neglected tropical disease human intestinal schistosomiasis. By focusing onS. mansoni in vivowith its broadly distributed sub-Saharan African snail intermediate host,Biomphalaria pfeifferi, we uncover new insights and basic knowledge of this host-parasite relationship that are critical for understanding schistosomiasis transmission. We show thatin vivostudies, particularly using field-derived specimens, provides a distinct view from the uniformed transcriptional responses traditionally seen fromin vitrostudies onS. mansoniandBiomphalariasnails. With the growing consensus that we need to supplement chemotherapy with other control methods, understanding howS. mansoniinteracts with its obligatory snail host becomes integral for future planning of control programs. The data provided within provides specific analysis on how the schistosomes successfully protect themselves from host defenses and the necessary transcriptional responses required for its amplifying asexual proliferation that result in human-infective cercariae.