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Cestode Taenia Multiceps Detailed Transcriptome Description of the Neglected Cestode Taenia multiceps Xuhang Wu1, Yan Fu1, Deying Yang1, Runhui Zhang1, Wanpeng Zheng1, Huaming Nie1,YueXie1, Ning Yan1, Guiying Hao1, Xiaobin Gu1, Shuxian Wang1, Xuerong Peng2, Guangyou Yang1* 1 Department of Parasitology, College of Veterinary Medicine, Sichuan Agricultural University, Ya’an, China, 2 Department of Chemistry, College of Life and Basic Science, Sichuan Agricultural University, Ya’an, China Abstract Background: The larval stage of Taenia multiceps, a global cestode, encysts in the central nervous system (CNS) of sheep and other livestock. This frequently leads to their death and huge socioeconomic losses, especially in developing countries. This parasite can also cause zoonotic infections in humans, but has been largely neglected due to a lack of diagnostic techniques and studies. Recent developments in next-generation sequencing provide an opportunity to explore the transcriptome of T. multiceps. Methodology/Principal Findings: We obtained a total of 31,282 unigenes (mean length 920 bp) using Illumina paired-end sequencing technology and a new Trinity de novo assembler without a referenced genome. Individual transcription molecules were determined by sequence-based annotations and/or domain-based annotations against public databases (Nr, UniprotKB/Swiss-Prot, COG, KEGG, UniProtKB/TrEMBL, InterPro and Pfam). We identified 26,110 (83.47%) unigenes and inferred 20,896 (66.8%) coding sequences (CDS). Further comparative transcripts analysis with other cestodes (Taenia pisiformis, Taenia solium, Echincoccus granulosus and Echincoccus multilocularis) and intestinal parasites (Trichinella spiralis, Ancylostoma caninum and Ascaris suum) showed that 5,100 common genes were shared among three Taenia tapeworms, 261 conserved genes were detected among five Taeniidae cestodes, and 109 common genes were found in four zoonotic intestinal parasites. Some of the common genes were genes required for parasite survival, involved in parasite-host interactions. In addition, we amplified two full-length CDS of unigenes from the common genes using RT-PCR. Conclusions/Significance: This study provides an extensive transcriptome of the adult stage of T. multiceps, and demonstrates that comparative transcriptomic investigations deserve to be further studied. This transcriptome dataset forms a substantial public information platform to achieve a fundamental understanding of the biology of T. multiceps, and helps in the identification of drug targets and parasite-host interaction studies. Citation: Wu X, Fu Y, Yang D, Zhang R, Zheng W, et al. (2012) Detailed Transcriptome Description of the Neglected Cestode Taenia multiceps. PLoS ONE 7(9): e45830. doi:10.1371/journal.pone.0045830 Editor: Geoffrey N. Gobert, Queensland Institute of Medical Research, Australia Received March 15, 2012; Accepted August 23, 2012; Published September 25, 2012 Copyright: ß 2012 Wu 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: This work was supported by the ‘‘Program for Changjiang Scholars and Innovative Research Team in University’’ (PCSIRT) (No. IRT0848). 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] Introduction through contaminated food or water [12]. The proglottids then release oncospheres in the intestine and penetrate the intestinal Taenia multiceps is a taeniid cestode, which inhabits the small mucosa and blood vessels. After reaching the brain through the intestine of dogs and other canids (foxes, wolves, and jackals), bloodstream, they will take 2–3 months to grow into a coenurus making these definitive hosts a widespread infection reservoir [1]. causing increased intracranial pressure. This will lead to the onset The coenurus (larva of T. multiceps) parasitizes the central nervous of clinical signs, such as ataxia, hypermetria, blindness, head system (CNS) of sheep, occasionally goats, deer, antelopes, deviation, headache, stumbling and paralysis [13–15]. Once the chamois, rabbits, hares and horses, and less commonly, cattle tissue of infected sheep or other livestock has been ingested by [2–5]. It frequently causes the death of infected animals, and can a definitive host, the lifecycle is completed, and the parasites lead to huge economic losses of sheep/goats, predominantly in develop into adult tapeworms in the small intestine of the host [5]. developing countries, such as those in Africa and southeastern Asia Together with this complex lifecycle, the specific immune [6]. The parasite can also cause zoonotic infections in humans, evasion traits of parasites and even the randomness of the infection leading to serious pathological conditions in humans, which occur make research and drug or vaccine programs for Taenia species more commonly than previously assumed [6–11]. very difficult; consequently, new methods to control this parasite The gravid proglottids of T. multiceps are discharged from are required. Although traditional methods of control (such as infected dogs and are ingested by intermediate hosts (including burning out the infected brain and spinal cord of sheep, or humans, especially in rural grazing areas where people raise sheep deworming infected dogs with anti-parasitic drugs) help to disrupt or other ungulates, and keep guard dogs in close proximity) PLOS ONE | www.plosone.org 1 September 2012 | Volume 7 | Issue 9 | e45830 Transcriptomic Analysis of Taenia multiceps the lifecycle of this parasite, its global distribution still includes 1,268 bp (Table 1). A total of 36,538 contigs (68.21%) were longer Europe [16–19], North America [8,9], Africa and Asia [6,20]. than 500 bp. To join further sequences and remove any Despite its global importance, available gene sequences for redundant sequences, contigs were clustered using the TIGR T. multiceps remain scarce. Currently, only 101 nucleotide Gene Indices clustering tools (TGICL). A total of 31,282 unigenes sequences and 103 proteins have been published on NCBI and were produced by the clustering, with an average length of 920 bp only the mitochondrial genome of T. multiceps has been sequenced and a N50 of 1,206 bp (Table 1). Of these, 20,123 unigenes [21]. To improve the control of this parasitic cestode, the (64.33%) were longer than 500 bp, and 9,504 unigenes (30.38%) identification of molecular targets to develop new effective anti- were longer than 1,000 bp. Short contigs and unigenes (less than parasitic drugs are necessary. Recent developments in next 300 bp) were removed, the maximum length of both contigs and generation sequencing (NGS) technologies [22–25] and recent unigenes was 11,875 bp (Table 1). The length distribution of these progress in bioinformatics, such as the new Trinity de novo contigs and unigenes is shown in Figure 1A. The gap distribution assembling program [26], make it possible to explore the of contigs and unigenes was analyzed to identify the data quality. fundamental biology of cestodes in far greater detail than currently All contigs and unigenes showed no gaps, thus demonstrating the available information, and are cheaper than the commonly used high quality of Trinity assembling (Figure 1B). Sanger sequencing technique [27]. To date, a fractionated transcriptome of the human parasite, Taenia solium cysticerca, has Annotation Against Public Databases been revealed by the ORESTES method [28], and a cDNA In order to obtain and validate sequence-based annotations for library has been constructed [29] with 30,700 ESTs available in all assembled unigenes, we employed Blastx for a sequence GenBank. Some vaccine and diagnostic targets were proposed similarity search against the Nr database (animal protein of Nr and from this study. However, further datasets generated by high- Drosophila protein of Nr databases), in addition to the Uni- throughput sequencing and comparative transcriptome analysis ProtKB/Swiss-Prot, UniProtKB/TrEMBL, COG, and KEGG could bring a more comprehensive understanding of parasite databases, with an e-value threshold of 1.025. The results biology. To our knowledge, the transcriptomes of Taenia pisiformis, indicated that out of 31,282 unigenes, a total of 17,618 (56.32%) T. solium, Echinococcus granulosus, Echinococcus multilocularis and unigenes were annotated against animal protein of Nr, 5,925 Hymenolepis microstoma by NGS technology have already been (18.94%) against Drosophila protein of Nr, 14,350 (45.87%) studied, but only T. pisiformis transcriptome dataset has been obtained annotations against UniProtKB/Swiss-Prot, 16,286 published [30,31]. Compared with nematodes [32–38] and (52.06%) against UniProtKB/TrEMBL, 6,653 (21.3%) received trematodes [39–42], published transcriptome data of cestodes by annotation against COG, and 11,645 (37.3%) against the KEGG NGS remain scarce. An improved understanding of the entire database (Table 1). Altogether, BLAST searches against Nr, molecular transcriptome of the adult stage of this cestode is UniProtKB/Swiss-Prot, UniProtKB/TrEMBL, COG and KEGG necessary. This can provide a platform to execute the identifica- databases identified 17,768 (56.80% of 31,282 unigenes) non- tion or validation of required genes and gene products in the redundant
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