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Comparative genomic analysis and phylogenetic position of Theileria equi.

ABSTRACT: 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.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.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.

SUBMITTER: Kappmeyer LS

PROVIDER: S-EPMC3505731 | biostudies-literature | 2012 Nov

REPOSITORIES: biostudies-literature

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Comparative genomic analysis and phylogenetic position of Theileria equi.

Kappmeyer Lowell S LS Thiagarajan Mathangi M Herndon David R DR Ramsay Joshua D JD Caler Elisabet E Djikeng Appolinaire A Gillespie Joseph J JJ Lau Audrey Ot AO Roalson Eric H EH Silva Joana C JC Silva Marta G MG Suarez Carlos E CE Ueti Massaro W MW Nene Vishvanath M VM Mealey Robert H RH Knowles Donald P DP Brayton Kelly A KA

BMC genomics 20121109

<h4>Background</h4>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 develo ...[more]

PMID: 23137308

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Project description:IntroductionStreptococcus equi subspecies equi (S. equi) is the causative agent of strangles, which is one of the most common and highly contagious respiratory infectious illnesses in horses. Streptococcus equi (S. equi) is a horse-specific pathogen that originated from the closely related zoonotic pathogen Streptococcus equi subspecies zooepidemicus (S. zooepidemicus). Despite decades of research, the movement of genetic material across host-restricted diseases remains a mystery.MethodsThree S. equi donkey isolates (HTP133, HTP232, and HT1112) were recently isolated from a strangles epidemic on donkey farms in China's Xinjiang Province. In this study, we performed a comprehensive comparative analysis of these isolates using whole genome sequencing and compared them to the published genomic sequences of equine strain S. equi 4047 to uncover evidence of genetic events that shaped the evolution of these donkey S. equi isolates' genomes.ResultsWhole genome sequencing indicated that both strains were closely related, with comparable gene compositions and a high rate of shared core genomes (1788-2004). Our comparative genomic study indicated that the genome structure is substantially conserved across three donkey strains; however, there are several rearrangements and inversions when compared to the horse isolate S. equi 4047. The virulence factors conveyed by genomic islands and prophages, in particular, played a key role in shaping the pathogenic capacity and genetic diversity of these S. equi strains. Furthermore, we discovered that the HT133 isolate had a strong colonization ability and increased motility; the HT1112 isolates had a significantly higher ability for antimicrobial resistance and biofilm formation, and the HT232 isolate gained pathogenic specialization by acquiring a bacteriophage encoding hyaluronate lyase.DiscussionIn summary, our findings show that genetic exchange across S. equi strains influences the development of the donkey S. equi genome, offering important genetic insights for future epidemiological studies of S. equi infection.

Project description:BackgroundThe apicomplexan hemoprotozoan parasite Theileria equi is one of the etiologic agents causing equine piroplasmosis, a disease of equines that is endemic throughout large parts of the world. Before 2009 the United States had been considered to be free of this parasite. Occasional cases had occurred but there was no evidence for endemic vector-borne transmission in the U.S. until a 2009 outbreak in Texas in which Dermacentor variabilis and Amblyomma cajennense were implicated as vectors. Although D. variabilis has previously been shown to be a competent laboratory vector, studies suggested A. cajennense was not a competent transstadial vector, even though the presence of this tick species on horses in South American is epidemiologicaly correlated with higher a prevalence of infection. In this study we tested the transstadial and intrastadial vector competence of D. variabilis and A. cajennense for T. equi.MethodsA tick passaged T. equi strain from the Texas outbreak and ticks colonized from engorged females collected off horses on the outbreak ranch in Texas were used for these studies. Nymph or adult ticks were fed on infected horses and transmission fed on naïve horses. Infections were tracked with PCR and serology, dissected tick tissues were tested with PCR.ResultsA. cajennense transmitted T. equi intrastadially when adult ticks acquired infection by feeding on an infected horse, and transmitted to a naïve host on subsequent reattachment and feeding. D. variabilis failed to transmit in the same experiment. Transstadial transmission was not successful for either tick species. PCR on DNA isolated from eggs of females that had fed on an infected horse suggests that there is no transovarial passage of this parasite by either tick species.ConclusionThis work confirms that ticks from the Texas population of A. cajennense are competent intrastadial vectors of T. equi. We propose that the most likely natural mode of transmission for this parasite/vector combination in the Texas outbreak would have been biological transmission resulting from adult male ticks moving between infected and uninfected horses. The intrastadial mode of transmission should be considered as one equally possible scenario whenever implicating vectors of T. equi.

Dataset Information

Comparative genomic analysis and phylogenetic position of Theileria equi.

Publications

Comparative genomic analysis and phylogenetic position of Theileria equi.

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