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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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) |
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Arctic medicine. Tropical medicine RC955-962 Public aspects of medicine RA1-1270 |
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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 |
work_keys_str_mv |
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