Eimeria genomics: Where are we now and where are we going?
Introduction
The word ‘genomics’ is widely considered to have appeared in 1986 (Kuska, 1998), with the first appearance of the term in the National Center for Biotechnology Information literature database appearing in 1987. By the year 2000 more than 1500 publications had appeared including the word ‘genomics’ as a searchable term, with 15,991 publications last year (2014). Many definitions of the term have been proposed, with a common theme being studies of the genome of an organism and genome-wide analysis of the genes it contains using DNA sequencing and bioinformatics methods. Progress in genomics led to publication of the first eukaryotic chromosome sequence in 1992, followed by the first full eukaryotic genome in 1996 (Oliver et al., 1992, Goffeau et al., 1996), but the roll out of genomics technologies has largely been constrained by the cost and availability of Sanger (or first generation) sequencing and the expertise required for analysis. As a consequence, genomics approaches were initially only accessible for the human genome and other model or medically relevant organisms. The advent of second or next generation sequencing technologies (NGS), providing faster, cheaper and higher throughput approaches, has unlocked genomics for use with veterinary and diagnostic purposes. While the rate of exploitation is not yet comparable with human and medical pathogen genomics, illustrated by greater fragmentation for most livestock and veterinary pathogen genomes (Table 1), sequence resources and associated opportunities are developing fast. Progress in genome sequencing and genome-wide analyses for the Eimeria species illustrates the impact of these advances and the opportunities which are only now becoming readily available.
Section snippets
Eimeria and the disease coccidiosis
Eimeria are obligate protozoan parasites which have evolved to exhibit immense diversity in host range including mammals, birds, reptiles, fish and amphibians, with each parasite species commonly defined by absolute host specificity (Jirku et al., 2009, Gibson-Kueh et al., 2011, Yang et al., 2012, Chapman et al., 2013, Jirku et al., 2013, Kvicerova and Hypsa, 2013). As a consequence there are likely to be many thousands of Eimeria species. Eimeria that infect wild vertebrates can become
Sequencing technologies
DNA sequencing by fragmentation or chain termination first appeared in the late 1970s with the latter, commonly referred to as Sanger sequencing, becoming dominant due to methodological advantage (Maxam and Gilbert, 1977, Sanger et al., 1977). The following 25 years saw considerable innovation and improvement to the Sanger sequencing technique and associated data analysis but limitations including requirements for minimum template quality and quantity, restricted throughput capacity and high
Application to eimerian genomes
Genome sequencing started for Eimeria in 2002, beginning with the reference Eimeria tenella Houghton strain (Chapman and Shirley, 2003). Prior to 2002 genomic resources were scarce, largely limited to Sanger sequencing reads covering the ribosomal DNA clusters, sporozoite and second generation merozoite expressed sequence tag (EST) cDNA reads, sequenced random amplified polymorphic DNA (RAPD) markers, and a panel of specific protein-coding genes including several kinases and microneme proteins (
Transcriptomic analyses
Eimerian parasites follow a strict faecal-oral life cycle which features three distinct phases and no intermediate host. The first phase, termed sporogony or sporulation, occurs outside of the host and includes asexual replication as the parasite develops from a single non-infectious unsporulated oocyst into an infective sporulated oocyst, containing eight sporozoites accommodated in pairs within four sporocysts. The second phase, known as schizogony or merogony, occurs within the host and
What next for Eimeria genomics?
The publication of genome sequences for all seven Eimeria species which infect chickens represented the culmination of more than a decade of work from a consortium of 20 institutions across ten countries (Reid et al., 2014). The provision of reference genome assemblies, combined with the reduced cost and greater power of NGS technologies, now provides enormous opportunity for genomics-led studies and diagnostics with these parasites. Access to a first mammalian-infecting Eimeria genome assembly
Applications for Eimeria genomics?
Addition of Eimeria to the ever-expanding club of sequenced genomes has dramatically expanded the scope for studies of biology, prophylaxis, therapy and vaccination. Comparison between genome assemblies representing related coccidians is straightforward and accessible using GeneDB, or ToxoDB within the EuPathDB resource (http://toxodb.org/toxo/http://toxodb.org/toxo/); (Gajria et al., 2008, Logan-Klumpler et al., 2012, Aurrecoechea et al., 2013). ToxoDB currently facilitates access to eight
Conclusions
The landmark publication of eight eimerian genome sequences in 2014 has provided a massive boost for studies with Eimeria, related apicomplexans and many protozoa. Given greater access to sequence data and the rapidly developing availability of NGS technologies with reduced cost, experimental limitations have now moved on to our capacity for data analysis and interpretation (Padmanabhan et al., 2013). Looking to the future improved bioinformatics pipelines will be required to improve
References (83)
- et al.
Developmental gene expression in Eimeria bovis
Mol. Biochem. Parasitol.
(1993) - et al.
EmaxDB: availability of a first draft genome sequence for the apicomplexan Eimeria maxima
Mol. Biochem. Parasitol.
(2012) - et al.
Securing poultry production from the ever-present Eimeria challenge
Trends Parasitol.
(2014) - et al.
A selective review of advances in coccidiosis research
Adv. Parasitol.
(2013) - et al.
A toolbox facilitating stable transfection of Eimeria species
Mol. Biochem. Parasitol.
(2008) - et al.
The molecular characterization of an Eimeria and Cryptosporidium detected in Asian seabass (Lates calcarifer) cultured in Vietnam
Vet. Parasitol.
(2011) - et al.
A genome-scale vector resource enables high-throughput reverse genetic screening in a malaria parasite
Cell Host Microbe
(2015) - et al.
World Association for the Advancement of Veterinary Parasitology (WAAVP) guidelines for evaluating the efficacy of anticoccidial drugs in chickens and turkeys
Vet. Parasitol.
(2004) - et al.
Evolutionary plasticity in coccidia – striking morphological similarity of unrelated coccidia (apicomplexa) from related hosts: Eimeria spp. from African and Asian Pangolins (Mammalia: Pholidota)
Protist
(2013) - et al.
Comparison of global transcriptional responses to primary and secondary Eimeria acervulina infections in chickens
Dev. Comp. Immunol.
(2010)
Adaptation of signature-tagged mutagenesis for Toxoplasma gondii: a negative screening strategy to isolate genes that are essential in restrictive growth conditions
Mol. Biochem. Parasitol.
Estimation of the economical effects of Eimeria infections in Estonian dairy herds using a stochastic model
Prev. Vet. Med.
A comparative transcriptome analysis reveals expression profiles conserved across three Eimeria spp. of domestic fowl and associated with multiple developmental stages
Int J. Parasitol.
The rhoptry proteome of Eimeria tenella sporozoites
Int. J. Parasitol.
Genomics and metagenomics in medical microbiology
J. Microbiol. Methods
Identification of virus-like particles in Eimeria stiedae
Mol. Biochem. Parasitol.
The Eimeria genome projects: a sequence of events
Trends Parasitol.
EtMIC4: a microneme protein from Eimeria tenella that contains tandem arrays of epidermal growth factor-like repeats and thrombospondin type-I repeats
Int. J. Parasitol.
Ten years of next-generation sequencing technology
Trends Genet.
A survey of genes in Eimeria tenella merozoites by EST sequencing
Int. J. Parasitol.
Stable transfection of Eimeria tenella: constitutive expression of the YFP-YFP molecule throughout the life cycle
Int. J. Parasitol.
Expressed sequence tags from Eimeria brunetti-preliminary analysis and functional annotation
Parasitol. Res.
Characterisation of full-length cDNA sequences provides insights into the Eimeria tenella transcriptome
BMC Genomics
EuPathDB: the eukaryotic pathogen database
Nucleic Acids Res.
QTL detection for coccidiosis (Eimeria tenella) resistance in a Fayoumi × Leghorn F(2) cross, using a medium-density SNP panel
Genet. Sel. Evol.
Comment on the review anticoccidial vaccines for broiler chickens: pathways to success by R.B. Williams (2002). Avian Pathology, 31, 317–353
Avian Pathol.
Toward the 1000 dollars human genome
Pharmacogenomics
Genetic mapping identifies novel highly protective antigens for an apicomplexan parasite
PLoS Pathog.
The influence of immunizing dose size and schedule on immunity to subsequent challenge with antigenically distinct strains of Eimeria maxima
Avian Pathol.
Systems-based analysis of the Sarcocystis neurona genome identifies pathways that contribute to a heteroxenous life cycle
MBio
Vaccination of chickens against coccidiosis ameliorates drug resistance in commercial poultry production
Int. J. Parasitol. Drugs Drug Resist.
The Houghton strain of Eimeria tenella: a review of the type strain selected for genome sequencing
Avian Pathol.
Poultry coccidiosis: recent advancements in control measures and vaccine development
Expert Rev. Vaccines
Analysis of differentially expressed genes in the precocious line of Eimeria maxima and its parent strain using suppression subtractive hybridization and cDNA microarrays
Parasitol. Res.
Sequence, expression and localization of calmodulin-domain protein kinases in Eimeria tenella and Eimeria maxima
Parasitology
A survey of the inter- and intraspecific RAPD markers of Eimeria spp. of the domestic fowl and the development of reliable diagnostic tools
Parasitol. Res.
ToxoDB: an integrated Toxoplasma gondii database resource
Nucleic Acids Res.
Next generation sequencing to detect variation in the Plasmodium falciparum circumsporozoite protein
Am. J. Trop. Med. Hyg.
Transposase mediated construction of RNA-seq libraries
Genome Res.
Life with 6000 genes
Science
The genome of Eimeria falciformis – reduction and specialization in a single host apicomplexan parasite
BMC Genomics
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