Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance

[Display omitted] •Genomic diversity between Theileria equi and Theileria haneyi is greater than Theileria parva and Theileria annulata.•Divergence time between T. equi and T. haneyi is greater than 33 million years.•Genomic diversity between T. equi and T. haneyi is not reflected in differences in...

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Veröffentlicht in:International journal for parasitology 2018-08, Vol.48 (9-10), p.679-690
Hauptverfasser: Knowles, Donald P., Kappmeyer, Lowell S., Haney, Darrell, Herndon, David R., Fry, Lindsay M., Munro, James B., Sears, Kelly, Ueti, Massaro W., Wise, Lauren N., Silva, Marta, Schneider, David A., Grause, Juanita, White, Stephen N., Tretina, Kyle, Bishop, Richard P., Odongo, David O., Pelzel-McCluskey, Angela M., Scoles, Glen A., Mealey, Robert H., Silva, Joana C.
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container_end_page 690
container_issue 9-10
container_start_page 679
container_title International journal for parasitology
container_volume 48
creator Knowles, Donald P.
Kappmeyer, Lowell S.
Haney, Darrell
Herndon, David R.
Fry, Lindsay M.
Munro, James B.
Sears, Kelly
Ueti, Massaro W.
Wise, Lauren N.
Silva, Marta
Schneider, David A.
Grause, Juanita
White, Stephen N.
Tretina, Kyle
Bishop, Richard P.
Odongo, David O.
Pelzel-McCluskey, Angela M.
Scoles, Glen A.
Mealey, Robert H.
Silva, Joana C.
description [Display omitted] •Genomic diversity between Theileria equi and Theileria haneyi is greater than Theileria parva and Theileria annulata.•Divergence time between T. equi and T. haneyi is greater than 33 million years.•Genomic diversity between T. equi and T. haneyi is not reflected in differences in pathogenesis.•The Equi merozoite antigen superfamily, present in T. equi, is also present in T. haneyi.•Diversity of Theileria in equids is exceptional and presents consequences for parasite surveillance. A novel apicomplexan parasite was serendipitously discovered in horses at the United States – Mexico border. Phylogenetic analysis based on 18S rDNA showed the erythrocyte-infective parasite to be related to, but distinct from, Theileria spp. in Africa, the most similar taxa being Theileria spp. from waterbuck and mountain zebra. The degree of sequence variability observed at the 18S rDNA locus also suggests the likely existence of additional cryptic species. Among described species, the genome of this novel equid Theileria parasite is most similar to that of Theileria equi, also a pathogen of horses. The estimated divergence time between the new Theileria sp. and T. equi, based on genomic sequence data, is greater than 33 million years. Average protein sequence divergence between them, at 23%, is greater than that of Theileria parva and Theileria annulata proteins, which is 18%. The latter two represent highly virulent Theileria spp. of domestic cattle, as well as of African and Asian wild buffalo, respectively, which differ markedly in pathology, host cell tropism, tick vector and geographical distribution. The extent of genome-wide sequence divergence, as well as significant morphological differences, relative to T. equi justify the classification of Theileria sp. as a new taxon. Despite the overall genomic divergence, the nine member equi merozoite antigen (EMA) superfamily, previously found as a multigene family only in T. equi, is also present in the novel parasite. Practically, significant sequence divergence in antigenic loci resulted in this undescribed Theileria sp. not being detectable using currently available diagnostic tests. Discovery of this novel species infective to equids highlights exceptional diversity within the genus Theileria, a finding with serious implications for apicomplexan parasite surveillance.
doi_str_mv 10.1016/j.ijpara.2018.03.010
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A novel apicomplexan parasite was serendipitously discovered in horses at the United States – Mexico border. Phylogenetic analysis based on 18S rDNA showed the erythrocyte-infective parasite to be related to, but distinct from, Theileria spp. in Africa, the most similar taxa being Theileria spp. from waterbuck and mountain zebra. The degree of sequence variability observed at the 18S rDNA locus also suggests the likely existence of additional cryptic species. Among described species, the genome of this novel equid Theileria parasite is most similar to that of Theileria equi, also a pathogen of horses. The estimated divergence time between the new Theileria sp. and T. equi, based on genomic sequence data, is greater than 33 million years. Average protein sequence divergence between them, at 23%, is greater than that of Theileria parva and Theileria annulata proteins, which is 18%. The latter two represent highly virulent Theileria spp. of domestic cattle, as well as of African and Asian wild buffalo, respectively, which differ markedly in pathology, host cell tropism, tick vector and geographical distribution. The extent of genome-wide sequence divergence, as well as significant morphological differences, relative to T. equi justify the classification of Theileria sp. as a new taxon. Despite the overall genomic divergence, the nine member equi merozoite antigen (EMA) superfamily, previously found as a multigene family only in T. equi, is also present in the novel parasite. Practically, significant sequence divergence in antigenic loci resulted in this undescribed Theileria sp. not being detectable using currently available diagnostic tests. 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A novel apicomplexan parasite was serendipitously discovered in horses at the United States – Mexico border. Phylogenetic analysis based on 18S rDNA showed the erythrocyte-infective parasite to be related to, but distinct from, Theileria spp. in Africa, the most similar taxa being Theileria spp. from waterbuck and mountain zebra. The degree of sequence variability observed at the 18S rDNA locus also suggests the likely existence of additional cryptic species. Among described species, the genome of this novel equid Theileria parasite is most similar to that of Theileria equi, also a pathogen of horses. The estimated divergence time between the new Theileria sp. and T. equi, based on genomic sequence data, is greater than 33 million years. Average protein sequence divergence between them, at 23%, is greater than that of Theileria parva and Theileria annulata proteins, which is 18%. The latter two represent highly virulent Theileria spp. of domestic cattle, as well as of African and Asian wild buffalo, respectively, which differ markedly in pathology, host cell tropism, tick vector and geographical distribution. The extent of genome-wide sequence divergence, as well as significant morphological differences, relative to T. equi justify the classification of Theileria sp. as a new taxon. Despite the overall genomic divergence, the nine member equi merozoite antigen (EMA) superfamily, previously found as a multigene family only in T. equi, is also present in the novel parasite. Practically, significant sequence divergence in antigenic loci resulted in this undescribed Theileria sp. not being detectable using currently available diagnostic tests. Discovery of this novel species infective to equids highlights exceptional diversity within the genus Theileria, a finding with serious implications for apicomplexan parasite surveillance.</description><subject>18S rDNA</subject><subject>Africa</subject><subject>amino acid sequences</subject><subject>Animals</subject><subject>antigens</subject><subject>buffaloes</subject><subject>cattle</subject><subject>cryptic species</subject><subject>diagnostic techniques</subject><subject>disease vectors</subject><subject>DNA, Protozoan - genetics</subject><subject>Equi merozoite antigen superfamily</subject><subject>Equids</subject><subject>Equus zebra</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>genetic variation</subject><subject>Genomics</subject><subject>geographical distribution</subject><subject>Horse Diseases - parasitology</subject><subject>Horses</subject><subject>loci</subject><subject>Male</subject><subject>merozoites</subject><subject>Mexico</subject><subject>monitoring</subject><subject>multigene family</subject><subject>nucleotide sequences</subject><subject>pathogens</subject><subject>Phylogenetic analysis</subject><subject>Phylogeny</subject><subject>Protein sequence divergence</subject><subject>proteins</subject><subject>ribosomal DNA</subject><subject>RNA, Ribosomal, 18S - genetics</subject><subject>Theileria</subject><subject>Theileria - genetics</subject><subject>Theileria - isolation &amp; purification</subject><subject>Theileria - pathogenicity</subject><subject>Theileria annulata</subject><subject>Theileria equi</subject><subject>Theileria parva</subject><subject>Theileriasis - parasitology</subject><subject>ticks</subject><subject>United States</subject><subject>Virulence</subject><issn>0020-7519</issn><issn>1879-0135</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc9u1DAQxiMEokvhDRDykUMTxnGyTjggoZZ_UiUu5Ww59riZVTZO7WTpvh8PVkdb4AYHy5bn-2bs75dlrzkUHPj23a6g3aSDLkrgTQGiAA5Psg1vZJsDF_XTbANQQi5r3p5lL2LcAfBaVNXz7Kxsm6auxHaT_bqiaPwBw5F5xzQb03lgcUJDGC_YTY80YCDNej3ikdhYpGJxwWh0aGY6IJs9w7uFbFL3dNsPac2R4b3BaSY_6oHd4uj3ZJhN8hBpPrKfNPc0srnHtbjEv3PeM9pPAxm9eiNzPjA9kfHpEu_1yNYfpxbI4hIOyTPo0eDL7JnTQ8RXj_t59uPzp5vLr_n19y_fLj9e56YGOefOIGqoSqO7UrtGdK7ellUn0LYaZed0XcvGVpZb60B2okXrWpsSk06CkFacZ29Pfafg7xaMs9qn9HB9BPolqpLzbSNLUcH_pVCXDbSJR5JWJ6kJPsaATk2B9jocFQe1olY7dUKtVtQKhEqok-3N44Sl26P9Y_rNNgk-nASYIjkQBhUT1BSXpZDYKevp3xMeAB4jwkk</recordid><startdate>201808</startdate><enddate>201808</enddate><creator>Knowles, Donald P.</creator><creator>Kappmeyer, Lowell S.</creator><creator>Haney, Darrell</creator><creator>Herndon, David R.</creator><creator>Fry, Lindsay M.</creator><creator>Munro, James B.</creator><creator>Sears, Kelly</creator><creator>Ueti, Massaro W.</creator><creator>Wise, Lauren N.</creator><creator>Silva, Marta</creator><creator>Schneider, David A.</creator><creator>Grause, Juanita</creator><creator>White, Stephen N.</creator><creator>Tretina, Kyle</creator><creator>Bishop, Richard P.</creator><creator>Odongo, David O.</creator><creator>Pelzel-McCluskey, Angela M.</creator><creator>Scoles, Glen A.</creator><creator>Mealey, Robert H.</creator><creator>Silva, Joana C.</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>201808</creationdate><title>Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance</title><author>Knowles, Donald P. ; Kappmeyer, Lowell S. ; Haney, Darrell ; Herndon, David R. ; Fry, Lindsay M. ; Munro, James B. ; Sears, Kelly ; Ueti, Massaro W. ; Wise, Lauren N. ; Silva, Marta ; Schneider, David A. ; Grause, Juanita ; White, Stephen N. ; Tretina, Kyle ; Bishop, Richard P. ; Odongo, David O. ; Pelzel-McCluskey, Angela M. ; Scoles, Glen A. ; Mealey, Robert H. ; Silva, Joana C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c507t-fceea042cab2af83bf5624b3ed9ae7bfa5578d4d1ddf07b39edf9d3447f7037d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>18S rDNA</topic><topic>Africa</topic><topic>amino acid sequences</topic><topic>Animals</topic><topic>antigens</topic><topic>buffaloes</topic><topic>cattle</topic><topic>cryptic species</topic><topic>diagnostic techniques</topic><topic>disease vectors</topic><topic>DNA, Protozoan - genetics</topic><topic>Equi merozoite antigen superfamily</topic><topic>Equids</topic><topic>Equus zebra</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>genetic variation</topic><topic>Genomics</topic><topic>geographical distribution</topic><topic>Horse Diseases - parasitology</topic><topic>Horses</topic><topic>loci</topic><topic>Male</topic><topic>merozoites</topic><topic>Mexico</topic><topic>monitoring</topic><topic>multigene family</topic><topic>nucleotide sequences</topic><topic>pathogens</topic><topic>Phylogenetic analysis</topic><topic>Phylogeny</topic><topic>Protein sequence divergence</topic><topic>proteins</topic><topic>ribosomal DNA</topic><topic>RNA, Ribosomal, 18S - genetics</topic><topic>Theileria</topic><topic>Theileria - genetics</topic><topic>Theileria - isolation &amp; purification</topic><topic>Theileria - pathogenicity</topic><topic>Theileria annulata</topic><topic>Theileria equi</topic><topic>Theileria parva</topic><topic>Theileriasis - parasitology</topic><topic>ticks</topic><topic>United States</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Knowles, Donald P.</creatorcontrib><creatorcontrib>Kappmeyer, Lowell S.</creatorcontrib><creatorcontrib>Haney, Darrell</creatorcontrib><creatorcontrib>Herndon, David R.</creatorcontrib><creatorcontrib>Fry, Lindsay M.</creatorcontrib><creatorcontrib>Munro, James B.</creatorcontrib><creatorcontrib>Sears, Kelly</creatorcontrib><creatorcontrib>Ueti, Massaro W.</creatorcontrib><creatorcontrib>Wise, Lauren N.</creatorcontrib><creatorcontrib>Silva, Marta</creatorcontrib><creatorcontrib>Schneider, David A.</creatorcontrib><creatorcontrib>Grause, Juanita</creatorcontrib><creatorcontrib>White, Stephen N.</creatorcontrib><creatorcontrib>Tretina, Kyle</creatorcontrib><creatorcontrib>Bishop, Richard P.</creatorcontrib><creatorcontrib>Odongo, David O.</creatorcontrib><creatorcontrib>Pelzel-McCluskey, Angela M.</creatorcontrib><creatorcontrib>Scoles, Glen A.</creatorcontrib><creatorcontrib>Mealey, Robert H.</creatorcontrib><creatorcontrib>Silva, Joana C.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>International journal for parasitology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Knowles, Donald P.</au><au>Kappmeyer, Lowell S.</au><au>Haney, Darrell</au><au>Herndon, David R.</au><au>Fry, Lindsay M.</au><au>Munro, James B.</au><au>Sears, Kelly</au><au>Ueti, Massaro W.</au><au>Wise, Lauren N.</au><au>Silva, Marta</au><au>Schneider, David A.</au><au>Grause, Juanita</au><au>White, Stephen N.</au><au>Tretina, Kyle</au><au>Bishop, Richard P.</au><au>Odongo, David O.</au><au>Pelzel-McCluskey, Angela M.</au><au>Scoles, Glen A.</au><au>Mealey, Robert H.</au><au>Silva, Joana C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance</atitle><jtitle>International journal for parasitology</jtitle><addtitle>Int J Parasitol</addtitle><date>2018-08</date><risdate>2018</risdate><volume>48</volume><issue>9-10</issue><spage>679</spage><epage>690</epage><pages>679-690</pages><issn>0020-7519</issn><eissn>1879-0135</eissn><abstract>[Display omitted] •Genomic diversity between Theileria equi and Theileria haneyi is greater than Theileria parva and Theileria annulata.•Divergence time between T. equi and T. haneyi is greater than 33 million years.•Genomic diversity between T. equi and T. haneyi is not reflected in differences in pathogenesis.•The Equi merozoite antigen superfamily, present in T. equi, is also present in T. haneyi.•Diversity of Theileria in equids is exceptional and presents consequences for parasite surveillance. A novel apicomplexan parasite was serendipitously discovered in horses at the United States – Mexico border. Phylogenetic analysis based on 18S rDNA showed the erythrocyte-infective parasite to be related to, but distinct from, Theileria spp. in Africa, the most similar taxa being Theileria spp. from waterbuck and mountain zebra. The degree of sequence variability observed at the 18S rDNA locus also suggests the likely existence of additional cryptic species. Among described species, the genome of this novel equid Theileria parasite is most similar to that of Theileria equi, also a pathogen of horses. The estimated divergence time between the new Theileria sp. and T. equi, based on genomic sequence data, is greater than 33 million years. Average protein sequence divergence between them, at 23%, is greater than that of Theileria parva and Theileria annulata proteins, which is 18%. The latter two represent highly virulent Theileria spp. of domestic cattle, as well as of African and Asian wild buffalo, respectively, which differ markedly in pathology, host cell tropism, tick vector and geographical distribution. The extent of genome-wide sequence divergence, as well as significant morphological differences, relative to T. equi justify the classification of Theileria sp. as a new taxon. Despite the overall genomic divergence, the nine member equi merozoite antigen (EMA) superfamily, previously found as a multigene family only in T. equi, is also present in the novel parasite. Practically, significant sequence divergence in antigenic loci resulted in this undescribed Theileria sp. not being detectable using currently available diagnostic tests. Discovery of this novel species infective to equids highlights exceptional diversity within the genus Theileria, a finding with serious implications for apicomplexan parasite surveillance.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>29885436</pmid><doi>10.1016/j.ijpara.2018.03.010</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0020-7519
ispartof International journal for parasitology, 2018-08, Vol.48 (9-10), p.679-690
issn 0020-7519
1879-0135
language eng
recordid cdi_proquest_miscellaneous_2116872340
source MEDLINE; Elsevier ScienceDirect Journals
subjects 18S rDNA
Africa
amino acid sequences
Animals
antigens
buffaloes
cattle
cryptic species
diagnostic techniques
disease vectors
DNA, Protozoan - genetics
Equi merozoite antigen superfamily
Equids
Equus zebra
Evolution, Molecular
Female
genetic variation
Genomics
geographical distribution
Horse Diseases - parasitology
Horses
loci
Male
merozoites
Mexico
monitoring
multigene family
nucleotide sequences
pathogens
Phylogenetic analysis
Phylogeny
Protein sequence divergence
proteins
ribosomal DNA
RNA, Ribosomal, 18S - genetics
Theileria
Theileria - genetics
Theileria - isolation & purification
Theileria - pathogenicity
Theileria annulata
Theileria equi
Theileria parva
Theileriasis - parasitology
ticks
United States
Virulence
title Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance
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