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The Genome of Eimeria Falciformis

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The Genome of Eimeria Falciformis Heitlinger et al. BMC Genomics 2014, 15:696 http://www.biomedcentral.com/1471-2164/15/696 RESEARCH ARTICLE Open Access The genome of Eimeria falciformis - reduction and specialization in a single host apicomplexan parasite Emanuel Heitlinger1, Simone Spork1, Richard Lucius1 and Christoph Dieterich2* Abstract Background: The phylum Apicomplexa comprises important unicellular human parasites such as Toxoplasma and Plasmodium. Eimeria is the largest and most diverse genus of apicomplexan parasites and some species of the genus are the causative agent of coccidiosis, a disease economically devastating in poultry. We report a complete genome sequence of the mouse parasite Eimeria falciformis. We assembled and annotated the genome sequence to study host-parasite interactions in this understudied genus in a model organism host. Results: The genome of E. falciformis is 44 Mb in size and contains 5,879 predicted protein coding genes. Comparative analysis of E. falciformis with Toxoplasma gondii shows an emergence and diversification of gene families associated with motility and invasion mainly at the level of the Coccidia. Many rhoptry kinases, among them important virulence factors in T. gondii, are absent from the E. falciformis genome. Surface antigens are divergent between Eimeria species. Comparisons with T. gondii showed differences between genes involved in metabolism, N-glycan and GPI-anchor synthesis. E. falciformis possesses a reduced set of transmembrane transporters and we suggest an altered mode of iron uptake in the genus Eimeria. Conclusions: Reduced diversity of genes required for host-parasite interaction and transmembrane transport allow hypotheses on host adaptation and specialization of a single host parasite. The E. falciformis genome sequence sheds light on the evolution of the Coccidia and helps to identify determinants of host-parasite interaction critical for drug and vaccine development. Background and Cyclospora caytanensis. The genus Eimeria does not The taxon Eimeria is the largest genus of the phylum infect humans, but is best known for species infecting Apicomplexa with more than 1,800 species [1]. The Api- domestic animals. Eimeria species cause > 2 billion US$ complexa are obligate intracellular parasites and the damage p. a. alone in the poultry industry [4]. Eimeriid phylum contains many well-known pathogens of humans parasites have single host life cycles and typically display a and livestock. Plasmodium species causing malaria can be strict host and tissue specificity. For example, the chicken regarded as the most threatening eukaryotes to human is parasitized by 7 species of Eimeria, each restricted to a [2]. The causative agent of toxoplasmosis, Toxoplasma special part of the intestine and causing severe, self- gondii, infects about a third of the worldwide human limiting infections [4]. population and causes pathology mostly in immunodefi- The development of E. falciformis Eimer, 1870 [5] is cient individuals and neonates [3]. restricted to crypt epithelial cells of the cecum and prox- Eimeriids dwell within cells of the intestine and intestine- imal colon of the mouse [6,7]. E. falciformis combines related tissues of vertebrates and invertebrates. The family the typical life cycle elements of parasites of the subclass comprises human pathogenic parasites like Isospora belli Coccidia (Figure 1): Infection occurs by ingestion of oo- cysts, containing eight haploid sporozoites. Sporozoites in- * Correspondence: [email protected] fect epithelial cells and undergo several rounds of asexual 2Computational RNA Biology and Ageing, Max Plank Institute for Biology of replication (“schizogony”), leading to very high numbers Ageing, Joseph-Stelzmann Straße 9b, 50913 Cologne, Germany of progeny called merozoites. These differentiate into Full list of author information is available at the end of the article © 2014 Heitlinger et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Heitlinger et al. BMC Genomics 2014, 15:696 Page 2 of 17 http://www.biomedcentral.com/1471-2164/15/696 Figure 1 Lifecycle of Eimeria compared to other Apicomplexans. The lifecycles of apicomplexan parasites are illustrated to highlight the differences in host and cell type specificity. Eimeria parasites have a single host lifecycle and show a strict tissue and cell type specificity. T. gondii can infect multiple hosts and different tissues and cell types. Sexual reproduction, however, is restricted to epithelial cells of cats. Plasmodium falciparum has an obligate two host lifecycle, proliferative stages are only found in humans, sexual reproduction takes place in mosquitoes. gametes (“gamogony”) that fuse to form diploid zygotes. the coherence of T. gondii as one generalist species, are After leaving the host via the feces in environmentally still not understood. resistant oocysts they undergo a reduction division Previously, high-quality genome sequences have been and mitotic divisions (“sporogony”) to yield the infective reported for T. gondii [13] and its very close relatives in sporozoites. As its host, the mouse, is among the best- the family Sarcocystidae Neospora caninum [14] and studied systems in biological research, the E. falciformis Hammondia hammondii [15]. In the family Eimeriidae, infection lends itself as a model to dissect facets of first studies of E. tenella chromosome I [16] and the de- Eimeria-host interaction [8-11]. scription of a database for the genome assembly of Eimeria Plasmodium is a Haemosporidian only distantly related maxima [17] were complemented by a large scale investi- to Eimeria and the Coccidia. T. gondii,theonlymember gation of all 7 species of Eimeria infecting chickens re- of the genus Toxoplasma, belongs to the same subclass cently [18]. Genome data has not been reported for any as the Eimeriidae, the Coccidia. Its life cycle shows Eimeria species infecting a host other than chicken. similarities to that of Eimeria in its feline definitive hosts, We determined a draft genome sequence of the mouse but in contrast to the specialist, it can infect >180 spe- parasite E. falciformis using a next generation sequen- cies of warm blooded animals as intermediate hosts, cing approach, to promote studies on the biology of including humans [3]. Due to this flexibility, this rela- Eimeriids. We performed comparative genomic analyses tively easy to handle parasite has become a well-studied and focused on the congener E. tenella and two more model organism that has greatly furthered the under- distant relatives, T. gondii and N. caninum, to infer the standing of apicomplexan biology. It has been argued that evolutionary history of genes playing roles in core pro- T. gondii needs its relatively large genome to adapt to cesses in these parasites. its wide variety of intermediate hosts, requiring for One such core process, the substrate dependent locomo- example flexibility with regard to host metabolism or tion of coccidian and haemosporidian parasites is called immune reposes. Interestingly, T. gondii has diverged gliding motility. An actin-dependent motor drives this into strains with different pathogenicity, supposedly process [19]. This movement is the basis for the invasion reflecting adaptation to the immune responses of its process, during which invasive stages of apicomplexan intermediate hosts [12]. The factors, which led to the and especially coccidian parasites establish themselves divergence of Eimeriids into specialist species and to in a parasitophorous vacuole. The secretion of surface Heitlinger et al. BMC Genomics 2014, 15:696 Page 3 of 17 http://www.biomedcentral.com/1471-2164/15/696 molecules from specialized apical organelles called micro- Organellar genomes nemes is triggered by cyclic nucleotide and calcium signal- Most apicomplexan parasites harbor a mitochondrion and ling and transduced by calcium dependent kinases. Other a rudimentary plastid organelle, the apicoplast, both of apical organelles, the rhoptries secrete kinases (Rhoptry which contain extra-nuclear DNA. We estimate the size kinases; RopKs) and pseudokinases interacting with the of both organellar genomes to 6.2 kb and ~33 kb, respect- host immune system [20]. ively. Both genomes are present in higher copy numbers Comparative genomics of the complete E. falciformis relative to the nuclear genome as estimated from sequen- genome allow a comprehensive view of the shared gene cing coverage (see Additional file 1). We predict ~180 repertoire among apicomplexan and coccidian parasites. copies per cell for the mitochondrial genome and 18–19 Our data for a rodent Eimeriid species allows identify- copies per cell for the apicoplast genome. ing genus specific processes and molecules. The presented The mitochondrial genome of E. falciformis is in good genome sequence thus provides a better understanding of agreement with GC content (34.5%) and size (6.2 kb) es- the biology of Eimeriids and a basis to establish E. falciformis timates for mitochondrial genomes of avian Eimeria species as a suitable model-parasite. [22]. For the protein encoding genes of the mitochondrial genome cytochrome
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