A transcriptomic analysis of Echinococcus granulosus larval stages

Background: The cestode Echinococcus granulosus the agent of cystic echinococcosis, a zoonosis affecting humans and domestic animals worldwide is an excellent model for the study of host-parasite cross-talk that interfaces with two mammalian hosts. To develop the molecular analysis of these interactions, we carried out an EST survey of E. granulosus larval stages. We report the salient features of this study with a focus on genes reflecting physiological adaptations of different parasite stages. Methodology/Principal Findings: We generated ,10,000 ESTs from two sets of full-length enriched libraries (derived from oligo-capped and trans-spliced cDNAs) prepared with three parasite materials: hydatid cyst wall, larval worms (protoscoleces), and pepsin/H-activated protoscoleces. The ESTs were clustered into 2700 distinct gene products. In the context of the biology of E. granulosus, our analyses reveal: (i) a diverse group of abundant long non-protein coding transcripts showing homology to a middle repetitive element (EgBRep) that could either be active molecular species or represent precursors of small RNAs (like piRNAs); (ii) an up-regulation of fermentative pathways in the tissue of the cyst wall; (iii) highly expressed thioland selenol-dependent antioxidant enzyme targets of thioredoxin glutathione reductase, the functional hub of redox metabolism in parasitic flatworms; (iv) candidate apomucins for the external layer of the tissuedwelling hydatid cyst, a mucin-rich structure that is critical for survival in the intermediate host; (v) a set of tetraspanins, a protein family that appears to have expanded in the cestode lineage; and (vi) a set of platyhelminth-specific gene products that may offer targets for novel pan-platyhelminth drug development. Conclusions/Significance: This survey has greatly increased the quality and the quantity of the molecular information on E. granulosus and constitutes a valuable resource for gene prediction on the parasite genome and for further genomic and proteomic analyses focused on cestodes and platyhelminths. Citation: Parkinson J, Wasmuth JD, Salinas G, Bizarro CV, Sanford C, et al. (2012) A Transcriptomic Analysis of Echinococcus granulosus Larval Stages: Implications for Parasite Biology and Host Adaptation. PLoS Negl Trop Dis 6(11): e1897. doi:10.1371/journal.pntd.0001897 Editor: Malcolm K. Jones, University of Queensland, Australia Received May 21, 2012; Accepted September 25, 2012; Published November 29, 2012 Copyright: 2012 Parkinson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: JP and JDW were funded by the Canadian Institute for Health Research (CIHR, http://www.cihr-irsc.gc.ca/; grant MOP84556), and CS by the Natural Sciences and Engineering Research Council of Canada (NSERC, http://www.nserc-crsng.gc.ca/; NSERC Discovery to JP; grant RGPIN 288266-04). EST sequencing in Brazil was supported by Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq, http://www.cnpq.br/). CVB was a recipient of a Coordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior (CAPES, http://www.capes.gov.br/) pre-doctoral fellowship. EST sequencing in the United Kingdom and MB were funded by the Wellcome Trust (http://www.wellcome.ac.uk/; grant 098051), that also supported CF (International Travelling Fellowship; Ref 061168) and RMM (Program Grant; Ref 090281). GS and CF received funds from the Programa para el Desarrollo de las Ciencias Básicas (PEDECIBA, http://www.pedeciba.edu.uy). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (CF); [email protected] (RMM) ¤a Current address: Department of Ecosystem and Public Health, Faculty of Veterinary Medicine, University of Calgary, Calgary, Canada ¤b Current address: Instituto Nacional de Ciência e Tecnologia em Tuberculose, Centro de Pesquisas em Biologia Molecular e Funcional, Pontifı́cia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brazil