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      Identification and analysis of Eimeria nieschulzi gametocyte genes reveal splicing events of gam genes and conserved motifs in the wall-forming proteins within the genus Eimeria (Coccidia, Apicomplexa) Translated title: L'identification et l'analyse des gènes des gamétocytes d' Eimeria nieschulzi révèlent des évènements d'épissage des gènes gam et des motifs conservés dans les protéines formant les parois chez le genre Eimeria (Coccidia, Apicomplexa)

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          Abstract

          The genus Eimeria (Apicomplexa, Coccidia) provides a wide range of different species with different hosts to study common and variable features within the genus and its species. A common characteristic of all known Eimeria species is the oocyst, the infectious stage where its life cycle starts and ends. In our study, we utilized Eimeria nieschulzi as a model organism. This rat-specific parasite has complex oocyst morphology and can be transfected and even cultivated in vitro up to the oocyst stage. We wanted to elucidate how the known oocyst wall-forming proteins are preserved in this rodent Eimeria species compared to other Eimeria. In newly obtained genomics data, we were able to identify different gametocyte genes that are orthologous to already known gam genes involved in the oocyst wall formation of avian Eimeria species. These genes appeared putatively as single exon genes, but cDNA analysis showed alternative splicing events in the transcripts. The analysis of the translated sequence revealed different conserved motifs but also dissimilar regions in GAM proteins, as well as polymorphic regions. The occurrence of an underrepresented gam56 gene version suggests the existence of a second distinct E. nieschulzi genotype within the E. nieschulzi Landers isolate that we maintain.

          Translated abstract

          Le genre Eimeria (Apicomplexa, Coccidia) fournit une large variété de différentes espèces avec différents hôtes pour étudier les caractéristiques communes et variables dans le genre et ses espèces. Une caractéristique commune de toutes les espèces connues d' Eimeria est l'oocyste, l'étape infectieuse par laquelle son cycle de vie commence et se termine. Dans notre étude, nous avons utilisé Eimeria nieschulzi comme organisme modèle. Ce parasite spécifique au rat présente une morphologie complexe de ses oocystes et peut être transfecté et même cultivé in vitro jusqu'au stade oocyste. Nous voulions élucider comment, dans cette espèce d' Eimeria de rongeurs, les protéines de formation de paroi d'oocystes connues sont préservées, en comparaison aux autres Eimeria. Dans les nouvelles données génomiques obtenues, nous avons pu identifier différents gènes de gamétocytes qui sont orthologues aux gènes gam déjà connus et impliqués dans la formation de la paroi d'oocystes d'espèces d' Eimeria aviaires. Ces gènes apparaissent possiblement comme des exons isolés, mais l'analyse par ADNc a montré des événements d'épissage alternatifs dans les transcripts. L'analyse de la séquence traduite a révélé différents motifs conservés et aussi des régions dissemblables dans les protéines GAM, ainsi que des régions polymorphes. L'existence d'une version sous-représentée du gène gam56 suggère l'existence d'un deuxième génotype distinct d' E. nieschulzi dans l'isolat E. nieschulzi Landers que nous entretenons.

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          Most cited references 44

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          RNA-Seq analysis of splicing in Plasmodium falciparum uncovers new splice junctions, alternative splicing and splicing of antisense transcripts

          Over 50% of genes in Plasmodium falciparum, the deadliest human malaria parasite, contain predicted introns, yet experimental characterization of splicing in this organism remains incomplete. We present here a transcriptome-wide characterization of intraerythrocytic splicing events, as captured by RNA-Seq data from four timepoints of a single highly synchronous culture. Gene model-independent analysis of these data in conjunction with publically available RNA-Seq data with HMMSplicer, an in-house developed splice site detection algorithm, revealed a total of 977 new 5′ GU-AG 3′ and 5 new 5′ GC-AG 3′ junctions absent from gene models and ESTs (11% increase to the current annotation). In addition, 310 alternative splicing events were detected in 254 (4.5%) genes, most of which truncate open reading frames. Splicing events antisense to gene models were also detected, revealing complex transcriptional arrangements within the parasite’s transcriptome. Interestingly, antisense introns overlap sense introns more than would be expected by chance, perhaps indicating a functional relationship between overlapping transcripts or an inherent organizational property of the transcriptome. Independent experimental validation confirmed over 30 new antisense and alternative junctions. Thus, this largest assemblage of new and alternative splicing events to date in Plasmodium falciparum provides a more precise, dynamic view of the parasite’s transcriptome.
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            The coccidian oocyst: a tough nut to crack!

            Coccidian parasites are transmitted between hosts by the ingestion of food or water contaminated with oocysts, followed by the release of infectious sporozoites and invasion of the gastro-intestinal tract. In the external environment, sporozoites are protected from desiccation and chemical disinfection by the oocyst wall. This unique structure guarantees successful disease transmission and is as vital to the coccidian parasite as the exoskeleton is to insects--without it they would die. Here, we revisit the early work and combine it with newer molecular data to describe our present understanding of the coccidian oocyst wall.
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              RNA Seq analysis of the Eimeria tenella gametocyte transcriptome reveals clues about the molecular basis for sexual reproduction and oocyst biogenesis

              Background The protozoan Eimeria tenella is a common parasite of chickens, causing avian coccidiosis, a disease of on-going concern to agricultural industries. The high prevalence of E. tenella can be attributed to the resilient oocyst stage, which is transmitted between hosts in the environment. As in related Coccidia, development of the eimerian oocyst appears to be dependent on completion of the parasite’s sexual cycle. RNA Seq transcriptome profiling offers insights into the mechanisms governing the biology of E. tenella sexual stages (gametocytes) and the potential to identify targets for blocking parasite transmission. Results Comparisons between the sequenced transcriptomes of E. tenella gametocytes and two asexual developmental stages, merozoites and sporozoites, revealed upregulated gametocyte transcription of 863 genes. Many of these genes code for proteins involved in coccidian sexual biology, such as oocyst wall biosynthesis and fertilisation, and some of these were characterised in more depth. Thus, macrogametocyte-specific expression and localisation was confirmed for two proteins destined for incorporation into the oocyst wall, as well as for a subtilisin protease and an oxidoreductase. Homologues of an oocyst wall protein and oxidoreductase were found in the related coccidian, Toxoplasma gondii, and shown to be macrogametocyte-specific. In addition, a microgametocyte gamete fusion protein, EtHAP2, was discovered. Conclusions The need for novel vaccine candidates capable of controlling coccidiosis is rising and this panel of gametocyte targets represents an invaluable resource for development of future strategies to interrupt parasite transmission, not just in Eimeria but in other Coccidia, including Toxoplasma, where transmission blocking is a relatively unexplored strategy. Electronic supplementary material The online version of this article (doi:10.1186/s12864-015-1298-6) contains supplementary material, which is available to authorized users.
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                Author and article information

                Journal
                Parasite
                Parasite
                parasite
                Parasite
                EDP Sciences
                1252-607X
                1776-1042
                2017
                6 December 2017
                : 24
                : ( publisher-idID: parasite/2017/01 )
                Affiliations
                Institute for Zoology, Technische Universität Dresden, Helmholtzstraße 10, 01062 Dresden Germany
                Author notes
                [* ]Corresponding author: kurth.michael@ 123456googlemail.com
                Article
                parasite170085 10.1051/parasite/2017049
                10.1051/parasite/2017049
                5718062
                29210668
                © S. Wiedmer et al., published by EDP Sciences, 2017

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 48, Pages: 13
                Categories
                Research Article

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