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Open Access Highly Accessed Research article

Comparative genomic analysis and phylogenetic position of Theileria equi

Lowell S Kappmeyer1, Mathangi Thiagarajan29, David R Herndon1, Joshua D Ramsay3, Elisabet Caler2, Appolinaire Djikeng4, Joseph J Gillespie56, Audrey OT Lau37, Eric H Roalson8, Joana C Silva6, Marta G Silva1, Carlos E Suarez1, Massaro W Ueti1, Vishvanath M Nene4, Robert H Mealey3, Donald P Knowles13 and Kelly A Brayton37*

Author Affiliations

1 Animal Disease Research Unit, Agricultural Research Service, USDA, Pullman, WA, 99164-7030, USA

2 J. Craig Venter Institute, Rockville, MD, 20850, USA

3 Department of Veterinary Microbiology & Pathology, Washington State University, Pullman, WA, 99164-7040, USA

4 International Livestock Research Institute, P.O. Box 30709, Nairobi, 00100, Kenya

5 Virginia Bioinformatics Institute at Virginia Tech, Blacksburg, VA, 24061, USA

6 Institute for Genome Sciences and Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, MD, 21201, USA

7 Paul G. Allen School for Global Animal Health, Washington State University, Pullman, WA, 99164-7040, USA

8 School of Biological Sciences, Washington State University, Pullman, WA, 99164-4236, USA

9 Current address: Frederick National Lab for Cancer Research, Rockville, MD, 20852, USA

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BMC Genomics 2012, 13:603  doi:10.1186/1471-2164-13-603

Published: 9 November 2012

Abstract

Background

Transmission of arthropod-borne apicomplexan parasites that cause disease and result in death or persistent infection represents a major challenge to global human and animal health. First described in 1901 as Piroplasma equi, this re-emergent apicomplexan parasite was renamed Babesia equi and subsequently Theileria equi, reflecting an uncertain taxonomy. Understanding mechanisms by which apicomplexan parasites evade immune or chemotherapeutic elimination is required for development of effective vaccines or chemotherapeutics. The continued risk of transmission of T. equi from clinically silent, persistently infected equids impedes the goal of returning the U. S. to non-endemic status. Therefore comparative genomic analysis of T. equi was undertaken to: 1) identify genes contributing to immune evasion and persistence in equid hosts, 2) identify genes involved in PBMC infection biology and 3) define the phylogenetic position of T. equi relative to sequenced apicomplexan parasites.

Results

The known immunodominant proteins, EMA1, 2 and 3 were discovered to belong to a ten member gene family with a mean amino acid identity, in pairwise comparisons, of 39%. Importantly, the amino acid diversity of EMAs is distributed throughout the length of the proteins. Eight of the EMA genes were simultaneously transcribed. As the agents that cause bovine theileriosis infect and transform host cell PBMCs, we confirmed that T. equi infects equine PBMCs, however, there is no evidence of host cell transformation. Indeed, a number of genes identified as potential manipulators of the host cell phenotype are absent from the T. equi genome. Comparative genomic analysis of T. equi revealed the phylogenetic positioning relative to seven apicomplexan parasites using deduced amino acid sequences from 150 genes placed it as a sister taxon to Theileria spp.

Conclusions

The EMA family does not fit the paradigm for classical antigenic variation, and we propose a novel model describing the role of the EMA family in persistence. T. equi has lost the putative genes for host cell transformation, or the genes were acquired by T. parva and T. annulata after divergence from T. equi. Our analysis identified 50 genes that will be useful for definitive phylogenetic classification of T. equi and closely related organisms.

Keywords:
Apicomplexa; Parasite; Vaccine; Horse; Vector-borne disease