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Population, Genetic, and Antigenic Diversity of the Apicomplexan Eimeria Tenella and Their Relevance to Vaccine Development

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Population, Genetic, and Antigenic Diversity of the Apicomplexan Eimeria Tenella and Their Relevance to Vaccine Development Population, genetic, and antigenic diversity of the PNAS PLUS apicomplexan Eimeria tenella and their relevance to vaccine development Damer P. Blakea,1, Emily L. Clarka,2, Sarah E. Macdonalda, Venkatachalam Thenmozhib, Krishnendu Kunduc, Rajat Gargc, Isa D. Jataud, Simeon Ayoadee, Fumiya Kawaharaf, Abdalgader Moftahg, Adam James Reidh, Ayotunde O. Adebamboe, Ramón Álvarez Zapatai, Arni S. R. Srinivasa Raoj,k, Kumarasamy Thangarajl, Partha S. Banerjeec, G. Dhinakar-Rajm, M. Ramanb, and Fiona M. Tomleya aPathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, AL9 7TA, United Kingdom; bDepartment of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, 600 007, Chennai, India; cDivision of Parasitology, Indian Veterinary Research Institute, Izatnagar, 243 122, Uttar Pradesh, India; dDepartment of Parasitology and Entomology, Faculty of Veterinary Medicine, Ahmadu Bello University, Zaria, Nigeria; eDepartment of Animal Breeding and Genetics, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria; fNippon Institute for Biological Science, Tokyo 198-0024, Japan; gSchool of Agriculture, Food and Rural Development, Newcastle University, Newcastle upon Tyne, NE1 7RU, United Kingdom; hParasite Genomics, Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridgeshire, CB10 1SA, United Kingdom; iFacultad de Agronomía Instituto de Producción Animal, Central University of Venezuela, Maracay, Venezuela; jDepartment of Biostatistics and Epidemiology Georgia Regents University, Augusta, GA 30912; kDepartment of Mathematics, Georgia Regents University, Augusta, GA 30912; lCouncil of Scientific and Industrial Research-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India; and mDepartment of Animal Biotechnology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai 600 007, India Edited by Jitender P. Dubey, US Department of Agriculture, Beltsville, MD, and approved August 21, 2015 (received for review April 1, 2015) The phylum Apicomplexa includes serious pathogens of humans and cines to control poultry coccidiosis (reviewed in ref. 5), it is now animals. Understanding the distribution and population structure of timely to investigate the extent, distribution, and dissemination of these protozoan parasites is of fundamental importance to explain genetic diversity in this parasite. disease epidemiology and develop sustainable controls. Predicting Sustainable food security is a major concern with the global the likely efficacy and longevity of subunit vaccines in field popula- human population set to exceed nine billion by 2050 (6). Poultry MICROBIOLOGY tions relies on knowledge of relevant preexisting antigenic diversity, are the most efficient source of animal-derived protein (7), and population structure, the likelihood of coinfection by genetically consequentially pathogens that compromise poultry production distinct strains, and the efficiency of cross-fertilization. All four of are reemerging as threats to the global food supply and as factors these factors have been investigated for Plasmodium species para- in human poverty (8, 9). Coccidiosis is a problem in many live- sites, revealing both clonal and panmictic population structures with stock systems; most notably, in chicken (broiler) production exceptional polymorphism associated with immunoprotective anti- seven different species of Eimeria cause serious intestinal disease gens such as apical membrane antigen 1 (AMA1). For the coccidian Toxoplasma gondii only genomic diversity and population structure Significance have been defined in depth so far; for the closely related Eimeria species, all four variables are currently unknown. Using Eimeria ten- ella, a major cause of the enteric disease coccidiosis, which exerts a Sixty billion chickens are produced worldwide each year, and all profound effect on chicken productivity and welfare, we determined areatriskfromEimeria, parasites that cause coccidiosis. Control population structure, genotype distribution, and likelihood of cross- relies widely on chemoprophylaxis, but pressure to reduce drug fertilization during coinfection and also investigated the extent of use in farming urges development of cost-effective vaccines. naturally occurring antigenic diversity for the E. tenella AMA1 homo- Antigens such as apical membrane antigen 1 (AMA1) offer log. Using genome-wide Sequenom SNP-based haplotyping, targeted promise as anticoccidial vaccine candidates, but experience with sequencing, and single-cell genotyping, we show that in this coccidian related apicomplexans such as Plasmodium, in which pre-existing the functionality of EtAMA1 appears to outweigh immune evasion. antigenic diversity and incompatible population structure have This result is in direct contrast to the situation in Plasmodium and undermined vaccine development, tempers confidence. Parasite most likely is underpinned by the biology of the direct and acute genotyping identified enormous region-specific variation in coccidian life cycle in the definitive host. haplotype diversity for Eimeria tenella but a contrastingly low level of polymorphism for EtAMA1. Although high levels of polyclonal Eimeria infection and hybridization indicate an Eimeria | coccidiosis | population structure | chickens | food security ability to disseminate vaccine resistance rapidly, the low level of EtAMA1 diversity promotes vaccine development. he phylum Apicomplexa contains protozoan parasites of great Tmedical and veterinary importance including Plasmodium, Author contributions: D.P.B., E.L.C., K.T., P.S.B., G.D.-R., M.R., and F.M.T. designed re- Toxoplasma,andEimeria species. Cost-effective vaccines and/or search; D.P.B., E.L.C., S.E.M., V.T., K.K., R.G., I.D.J., S.A., F.K., A.M., A.J.R., A.O.A., R.Á.Z., drugs are urgently required to control the diseases caused by these and A.S.R.S.R. performed research; V.T., K.K., R.G., I.D.J., S.A., F.K., A.M., A.O.A., R.Á.Z., P.S.B., G.D.-R., and M.R. contributed new reagents/analytic tools; D.P.B. and E.L.C. ana- pathogens, but their complex life cycles and naturally occurring lyzed data; and D.P.B., A.S.R.S.R., K.T., and F.M.T. wrote the paper. genetic polymorphism makes the development of such vaccines an The authors declare no conflict of interest. extremely difficult task. For Plasmodium species and Toxoplasma This article is a PNAS Direct Submission. gondii, in-depth studies have defined genetic diversity and pop- Freely available online through the PNAS open access option. ulation structures in many regions and populations, with de- – Data deposition: The sequences reported in this paper have been deposited in the scriptions ranging from clonality to panmixia (e.g., refs. 1 3). For GenBank database (accession nos. LN609976–LN610031 and LN626984–LN626991). Eimeria it is widely perceived that species occurrence has been 1To whom correspondence should be addressed. Email: [email protected]. established and that the risks posed are well understood, but 2Present address: The Roslin Institute, The University of Edinburgh, Easter Bush, Midlo- population structures within field populations are unclear, and the thian, EH25 9RG, United Kingdom. occurrence of genetic diversity is unexplored (4). Given the recent This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. progress in identifying antigens for inclusion in novel subunit vac- 1073/pnas.1506468112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1506468112 PNAS | Published online September 9, 2015 | E5343–E5350 Downloaded by guest on September 26, 2021 that compromises economic productivity and animal welfare, with the LCH2 and Weybridge (United Kingdom.), Beltsville incurring global costs in excess of $3 billion every year (10, 11). and Wisconsin (United States), and Nippon-2 (Nt2; Japan) Disease control relies on the use of in-feed drugs, but multidrug E. tenella strains revealed Jaccard indices of 0.912, 0.967, 0.956, resistant parasites are ubiquitous, and concerns about residues 0.914, and 0.873, respectively. Using these data, we selected the are widespread (12). Live anticoccidial vaccines have been used Wisconsin and Nt2 strains for next-generation sequencing (Illu- in small sectors of the poultry industry for more than 50 y with no mina), as described previously (13). The sequences are available evidence of parasite evolution toward resistance/immune escape from the European Nucleotide Archive under the accession (11). Examples of naturally occurring genetic diversity have been number PRJEB4009. Using these resources, we identified SNPs. reliably overcome by the inclusion of more than one “strain” of a First, sequences covering a panel of genes with known chromo- single species in some vaccine formulations (11). Each Eimeria somal locations were selected to provide an even dispersal of species expresses between 6,000 and 9,000 proteins throughout SNPs across the 14 E. tenella chromosomes (Dataset S1) (13, 17). its lifecycle (13), exposing the host to a complex portfolio of Additional SNPs were selected across chromosomes 1 and 2, antigens. Genetic mapping studies with Eimeria maxima in- including two to four SNPs in each repeat-rich (R) and repeat- dicated that at least six loci associate absolutely with suscepti- poor (P) region (Dataset S1) (13, 18). In total, 55 SNPs were bility to strong natural immune responses, and additional loci selected, incorporated into two Sequenom MassARRAY multi- under partial
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