Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.

Theileria parva is an economically important, intracellular, tick-transmitted parasite of cattle. A live vaccine against the parasite is effective against challenge from cattle-transmissible T. parva but not against genotypes originating from the African Cape buffalo, a major wildlife reservoir, pro...

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Autores principales: Nicholas C Palmateer, Kyle Tretina, Joshua Orvis, Olukemi O Ifeonu, Jonathan Crabtree, Elliott Drabék, Roger Pelle, Elias Awino, Hanzel T Gotia, James B Munro, Luke Tallon, W Ivan Morrison, Claudia A Daubenberger, Vish Nene, Donald P Knowles, Richard P Bishop, Joana C Silva
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spelling oai:doaj.org-article:8f70a77d240e4115906cbd29836599c82021-11-25T06:33:32ZCapture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.1935-27271935-273510.1371/journal.pntd.0008781https://doaj.org/article/8f70a77d240e4115906cbd29836599c82020-10-01T00:00:00Zhttps://doi.org/10.1371/journal.pntd.0008781https://doaj.org/toc/1935-2727https://doaj.org/toc/1935-2735Theileria parva is an economically important, intracellular, tick-transmitted parasite of cattle. A live vaccine against the parasite is effective against challenge from cattle-transmissible T. parva but not against genotypes originating from the African Cape buffalo, a major wildlife reservoir, prompting the need to characterize genome-wide variation within and between cattle- and buffalo-associated T. parva populations. Here, we describe a capture-based target enrichment approach that enables, for the first time, de novo assembly of nearly complete T. parva genomes derived from infected host cell lines. This approach has exceptionally high specificity and sensitivity and is successful for both cattle- and buffalo-derived T. parva parasites. De novo genome assemblies generated for cattle genotypes differ from the reference by ~54K single nucleotide polymorphisms (SNPs) throughout the 8.31 Mb genome, an average of 6.5 SNPs/kb. We report the first buffalo-derived T. parva genome, which is ~20 kb larger than the genome from the reference, cattle-derived, Muguga strain, and contains 25 new potential genes. The average non-synonymous nucleotide diversity (πN) per gene, between buffalo-derived T. parva and the Muguga strain, was 1.3%. This remarkably high level of genetic divergence is supported by an average Wright's fixation index (FST), genome-wide, of 0.44, reflecting a degree of genetic differentiation between cattle- and buffalo-derived T. parva parasites more commonly seen between, rather than within, species. These findings present clear implications for vaccine development, further demonstrated by the ability to assemble nearly all known antigens in the buffalo-derived strain, which will be critical in design of next generation vaccines. The DNA capture approach used provides a clear advantage in specificity over alternative T. parva DNA enrichment methods used previously, such as those that utilize schizont purification, is less labor intensive, and enables in-depth comparative genomics in this apicomplexan parasite.Nicholas C PalmateerKyle TretinaJoshua OrvisOlukemi O IfeonuJonathan CrabtreeElliott DrabékRoger PelleElias AwinoHanzel T GotiaJames B MunroLuke TallonW Ivan MorrisonClaudia A DaubenbergerVish NeneDonald P KnowlesRichard P BishopJoana C SilvaPublic Library of Science (PLoS)articleArctic medicine. Tropical medicineRC955-962Public aspects of medicineRA1-1270ENPLoS Neglected Tropical Diseases, Vol 14, Iss 10, p e0008781 (2020)
institution DOAJ
collection DOAJ
language EN
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
Nicholas C Palmateer
Kyle Tretina
Joshua Orvis
Olukemi O Ifeonu
Jonathan Crabtree
Elliott Drabék
Roger Pelle
Elias Awino
Hanzel T Gotia
James B Munro
Luke Tallon
W Ivan Morrison
Claudia A Daubenberger
Vish Nene
Donald P Knowles
Richard P Bishop
Joana C Silva
Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
description Theileria parva is an economically important, intracellular, tick-transmitted parasite of cattle. A live vaccine against the parasite is effective against challenge from cattle-transmissible T. parva but not against genotypes originating from the African Cape buffalo, a major wildlife reservoir, prompting the need to characterize genome-wide variation within and between cattle- and buffalo-associated T. parva populations. Here, we describe a capture-based target enrichment approach that enables, for the first time, de novo assembly of nearly complete T. parva genomes derived from infected host cell lines. This approach has exceptionally high specificity and sensitivity and is successful for both cattle- and buffalo-derived T. parva parasites. De novo genome assemblies generated for cattle genotypes differ from the reference by ~54K single nucleotide polymorphisms (SNPs) throughout the 8.31 Mb genome, an average of 6.5 SNPs/kb. We report the first buffalo-derived T. parva genome, which is ~20 kb larger than the genome from the reference, cattle-derived, Muguga strain, and contains 25 new potential genes. The average non-synonymous nucleotide diversity (πN) per gene, between buffalo-derived T. parva and the Muguga strain, was 1.3%. This remarkably high level of genetic divergence is supported by an average Wright's fixation index (FST), genome-wide, of 0.44, reflecting a degree of genetic differentiation between cattle- and buffalo-derived T. parva parasites more commonly seen between, rather than within, species. These findings present clear implications for vaccine development, further demonstrated by the ability to assemble nearly all known antigens in the buffalo-derived strain, which will be critical in design of next generation vaccines. The DNA capture approach used provides a clear advantage in specificity over alternative T. parva DNA enrichment methods used previously, such as those that utilize schizont purification, is less labor intensive, and enables in-depth comparative genomics in this apicomplexan parasite.
format article
author Nicholas C Palmateer
Kyle Tretina
Joshua Orvis
Olukemi O Ifeonu
Jonathan Crabtree
Elliott Drabék
Roger Pelle
Elias Awino
Hanzel T Gotia
James B Munro
Luke Tallon
W Ivan Morrison
Claudia A Daubenberger
Vish Nene
Donald P Knowles
Richard P Bishop
Joana C Silva
author_facet Nicholas C Palmateer
Kyle Tretina
Joshua Orvis
Olukemi O Ifeonu
Jonathan Crabtree
Elliott Drabék
Roger Pelle
Elias Awino
Hanzel T Gotia
James B Munro
Luke Tallon
W Ivan Morrison
Claudia A Daubenberger
Vish Nene
Donald P Knowles
Richard P Bishop
Joana C Silva
author_sort Nicholas C Palmateer
title Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
title_short Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
title_full Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
title_fullStr Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
title_full_unstemmed Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
title_sort capture-based enrichment of theileria parva dna enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity.
publisher Public Library of Science (PLoS)
publishDate 2020
url https://doaj.org/article/8f70a77d240e4115906cbd29836599c8
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