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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Main Authors: Palmateer, N.C., Tretina, Kyle, Orvis, J., Ifeonu, O.O., Crabtree, J., Drabék, E., Pelle, Roger, Awino, Elias, Gotia, H.T., Munro, James B., Tallon, L., Morrison, W.I., Daubenberger, C.A., Nene, Vishvanath M., Knowles, Donald P., Bishop, Richard P., Silva, Joana C.
Format: Journal Article
Language:Inglés
Published: Public Library of Science 2020
Subjects:
Online Access:https://hdl.handle.net/10568/110042
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author Palmateer, N.C.
Tretina, Kyle
Orvis, J.
Ifeonu, O.O.
Crabtree, J.
Drabék, E.
Pelle, Roger
Awino, Elias
Gotia, H.T.
Munro, James B.
Tallon, L.
Morrison, W.I.
Daubenberger, C.A.
Nene, Vishvanath M.
Knowles, Donald P.
Bishop, Richard P.
Silva, Joana C.
author_browse Awino, Elias
Bishop, Richard P.
Crabtree, J.
Daubenberger, C.A.
Drabék, E.
Gotia, H.T.
Ifeonu, O.O.
Knowles, Donald P.
Morrison, W.I.
Munro, James B.
Nene, Vishvanath M.
Orvis, J.
Palmateer, N.C.
Pelle, Roger
Silva, Joana C.
Tallon, L.
Tretina, Kyle
author_facet Palmateer, N.C.
Tretina, Kyle
Orvis, J.
Ifeonu, O.O.
Crabtree, J.
Drabék, E.
Pelle, Roger
Awino, Elias
Gotia, H.T.
Munro, James B.
Tallon, L.
Morrison, W.I.
Daubenberger, C.A.
Nene, Vishvanath M.
Knowles, Donald P.
Bishop, Richard P.
Silva, Joana C.
author_sort Palmateer, N.C.
collection Repository of Agricultural Research Outputs (CGSpace)
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.
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spelling CGSpace1100422025-01-28T07:08:05Z Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity Palmateer, N.C. Tretina, Kyle Orvis, J. Ifeonu, O.O. Crabtree, J. Drabék, E. Pelle, Roger Awino, Elias Gotia, H.T. Munro, James B. Tallon, L. Morrison, W.I. Daubenberger, C.A. Nene, Vishvanath M. Knowles, Donald P. Bishop, Richard P. Silva, Joana C. cattle livestock genomics infectious diseases 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. 2020-10-29 2020-11-03T21:20:45Z 2020-11-03T21:20:45Z Journal Article https://hdl.handle.net/10568/110042 en Open Access Public Library of Science Palmateer, N.C., Tretina, K., Orvis, J., Ifeonu, O.O., Crabtree, J., Drabék, E., Pelle, R., Awino, E., Gotia, H.T., Munro, J.B., Tallon, L., Morrison, W.I., Daubenberger, C.A., Nene, V., Knowles, D.P., Bishop, R.P. and Silva, J.C. 2020. Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity. PLOS Neglected Tropical Diseases 14(10): e0008781.
spellingShingle cattle
livestock
genomics
infectious diseases
Palmateer, N.C.
Tretina, Kyle
Orvis, J.
Ifeonu, O.O.
Crabtree, J.
Drabék, E.
Pelle, Roger
Awino, Elias
Gotia, H.T.
Munro, James B.
Tallon, L.
Morrison, W.I.
Daubenberger, C.A.
Nene, Vishvanath M.
Knowles, Donald P.
Bishop, Richard P.
Silva, Joana C.
Capture-based enrichment of Theileria parva DNA enables full genome assembly of first buffalo-derived strain and reveals exceptional intra-specific genetic diversity
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_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_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_sort capture based enrichment of theileria parva dna enables full genome assembly of first buffalo derived strain and reveals exceptional intra specific genetic diversity
topic cattle
livestock
genomics
infectious diseases
url https://hdl.handle.net/10568/110042
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