Population, genetic, and antigenic diversity of the apicomplexan Eimeria tenella and their relevance to vaccine development.
The phylum Apicomplexa includes serious pathogens of humans and animals. Understanding the distribution and population structure of these protozoan parasites is of fundamental importance to explain disease epidemiology and develop sustainable controls. Predicting the likely efficacy and longevity of subunit vaccines in field populations relies on knowledge of relevant preexisting antigenic diversity, population structure, the likelihood of coinfection by genetically distinct strains, and the efficiency of cross-fertilization. All four of these factors have been investigated for Plasmodium species parasites, revealing both clonal and panmictic population structures with exceptional polymorphism associated with immunoprotective antigens such as apical membrane antigen 1 (AMA1). For the coccidian Toxoplasma gondii only genomic diversity and population structure have been defined in depth so far; for the closely related Eimeria species, all four variables are currently unknown. Using Eimeria tenella, a major cause of the enteric disease coccidiosis, which exerts a profound effect on chicken productivity and welfare, we determined population structure, genotype distribution, and likelihood of cross-fertilization during coinfection and also investigated the extent of naturally occurring antigenic diversity for the E. tenella AMA1 homolog. Using genome-wide Sequenom SNP-based haplotyping, targeted sequencing, and single-cell genotyping, we show that in this coccidian the functionality of EtAMA1 appears to outweigh immune evasion. This result is in direct contrast to the situation in Plasmodium and most likely is underpinned by the biology of the direct and acute coccidian life cycle in the definitive host.
Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, AL9 7TA, United Kingdom; dblake@rvc.ac.uk.
Damer P
http://orcid.org/0000-0003-1077-2306
DP
Blake
Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, AL9 7TA, United Kingdom;
Emily L
EL
Clark
Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, AL9 7TA, United Kingdom;
Sarah E
SE
Macdonald
Department of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, 600 007, Chennai, India;
Venkatachalam
V
Thenmozhi
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, 243 122, Uttar Pradesh, India;
Krishnendu
K
Kundu
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, 243 122, Uttar Pradesh, India;
Rajat
R
Garg
Department of Parasitology and Entomology, Faculty of Veterinary Medicine, Ahmadu Bello University, Zaria, Nigeria;
Isa D
ID
Jatau
Department of Animal Breeding and Genetics, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria;
Simeon
S
Ayoade
Nippon Institute for Biological Science, Tokyo 198-0024, Japan;
Fumiya
F
Kawahara
School of Agriculture, Food and Rural Development, Newcastle University, Newcastle upon Tyne, NE1 7RU, United Kingdom;
Abdalgader
A
Moftah
Parasite Genomics, Wellcome Trust Sanger Institute, Genome Campus, Hinxton, Cambridgeshire, CB10 1SA, United Kingdom;
Adam James
AJ
Reid
Department of Animal Breeding and Genetics, Federal University of Agriculture, Abeokuta, Ogun State, Nigeria;
Ayotunde O
AO
Adebambo
Facultad de Agronomía Instituto de Producción Animal, Central University of Venezuela, Maracay, Venezuela;
Ramón
R
Álvarez Zapata
Department of Biostatistics and Epidemiology Georgia Regents University, Augusta, GA 30912; Department of Mathematics, Georgia Regents University, Augusta, GA 30912;
Arni S R
AS
Srinivasa Rao
Council of Scientific and Industrial Research-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India;
Kumarasamy
K
Thangaraj
Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, 243 122, Uttar Pradesh, India;
Partha S
PS
Banerjee
Department of Animal Biotechnology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, Chennai 600 007, India.
G
G
Dhinakar-Raj
Department of Veterinary Parasitology, Madras Veterinary College, Tamil Nadu Veterinary and Animal Sciences University, 600 007, Chennai, India;
M
M
Raman
Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hertfordshire, AL9 7TA, United Kingdom;
Fiona M
FM
Tomley
D000818:Animals; D000940:Antigenic Variation; D000953:Antigens, Protozoan / Q000276:immunology; D001483:Base Sequence; D002645:Chickens / Q000469:parasitology; D003048:Coccidiosis / Q000469:parasitology; D003433:Crosses, Genetic; D016786:Eimeria tenella / Q000235:genetics* / Q000276:immunology*; D005243:Feces; D014644:Genetic Variation; D005828:Genetics, Population; D005838:Genotype; D005843:Geography; D008969:Molecular Sequence Data; D033661:Oocysts; D010802:Phylogeny; D010961:Plasmodium / Q000235:genetics / Q000276:immunology; D020641:Polymorphism, Single Nucleotide; D011201:Poultry Diseases / Q000469:parasitology; D016052:Protozoan Vaccines
D000953:Antigens, Protozoan; D016052:Protozoan Vaccines
Eimeria; chickens; coccidiosis; food security; population structure