The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction
- Autores
- Jackson, Andrew P.; Otto, Thomas D.; Darby, Alistair; Ramaprasad, Abhinay; Xia, Dong; Echaide, Ignacio Eduardo; Farber, Marisa Diana; Gahlot, Sunayna; Gamble, John; Gupta, Dinesh; Gupta, Yask; Jackson, Louise; Malandrin, Laurence; Malas, Tareq B.; Moussa, Ehab; Nair, Mridul; Reid, Adam J.; Sanders, Mandy; Sharma, Jyotsna; Tracey, Alan; Quail, Mike A.; Weir, William; Wastling, Jonathan M.; Hall, Neil; Willadsen, Peter; Lingelbach, Klaus; Shiels, Brian; Tait, Andy; Berriman, Matt; Allred, David R.; Pain, Arnab
- Año de publicación
- 2014
- Idioma
- inglés
- Tipo de recurso
- artículo
- Estado
- versión publicada
- Descripción
- Babesia spp. are tick-borne, intraerythrocytic hemoparasites that use antigenic variation to resist host immunity, through sequential modification of the parasite-derived variant erythrocyte surface antigen (VESA) expressed on the infected red blood cell surface. We identified the genomic processes driving antigenic diversity in genes encoding VESA (ves1) through comparative analysis within and between three Babesia species, (B. bigemina, B. divergens and B. bovis). Ves1 structure diverges rapidly after speciation, notably through the evolution of shortened forms (ves2) from 5´ ends of canonical ves1 genes. Phylogenetic analyses show that ves1 genes are transposed between loci routinely, whereas ves2 genes are not. Similarly, analysis of sequence mosaicism shows that recombination drives variation in ves1 sequences, but less so for ves2, indicating the adoption of different mechanisms for variation of the two families. Proteomic analysis of the B. bigemina PR isolate shows that two dominant VESA1 proteins are expressed in the population, whereas numerous VESA2 proteins are co-expressed, consistent with differential transcriptional regulation of each family. Hence, VESA2 proteins are abundant and previously unrecognized elements of Babesia biology, with evolutionary dynamics consistently different to those of VESA1, suggesting that their functions are distinct.
Fil: Jackson, Andrew P.. University of Liverpool; Reino Unido
Fil: Otto, Thomas D.. Wellcome Trust Sanger Institute; Reino Unido
Fil: Darby, Alistair. University of Liverpool; Reino Unido
Fil: Ramaprasad, Abhinay. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Xia, Dong. University of Liverpool; Reino Unido
Fil: Echaide, Ignacio Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Santa Fe. Estación Experimental Agropecuaria Rafaela; Argentina
Fil: Farber, Marisa Diana. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Gahlot, Sunayna. International Centre for Genetic Engineering and Biotechnology; India
Fil: Gamble, John. Wellcome Trust Sanger Institute; Reino Unido
Fil: Gupta, Dinesh. International Centre for Genetic Engineering and Biotechnology; India
Fil: Gupta, Yask. International Centre for Genetic Engineering and Biotechnology; India
Fil: Jackson, Louise. Biosecurity Sciences Laboratory. Department of Agriculture, Fisheries and Forestry; Australia
Fil: Malandrin, Laurence. Institut National de la Recherche Agronomique; Francia. Oniris. Research Unit Biology, Epidemiology and Risk Analysis in Animal Health; Francia
Fil: Malas, Tareq B.. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Moussa, Ehab. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Nair, Mridul. King Abdullah University of Science and Technology; Arabia Saudita
Fil: Reid, Adam J.. Wellcome Trust Sanger Institute; Reino Unido
Fil: Sanders, Mandy. Wellcome Trust Sanger Institute; Reino Unido
Fil: Sharma, Jyotsna. Universitat Phillips; Alemania
Fil: Tracey, Alan. Wellcome Trust Sanger Institute; Reino Unido
Fil: Quail, Mike A.. Wellcome Trust Sanger Institute; Reino Unido
Fil: Weir, William. Universitat Phillips; Alemania
Fil: Wastling, Jonathan M.. University of Liverpool; Reino Unido
Fil: Hall, Neil. University of Liverpool; Reino Unido
Fil: Willadsen, Peter. Oniris. Research Unit Biology, Epidemiology and Risk Analysis in Animal Health; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Lingelbach, Klaus. Universitat Phillips; Alemania
Fil: Shiels, Brian. University of Glasgow; Reino Unido
Fil: Tait, Andy. University of Glasgow; Reino Unido
Fil: Berriman, Matt. Wellcome Trust Sanger Institute; Reino Unido
Fil: Allred, David R.. University of Florida; Estados Unidos
Fil: Pain, Arnab. King Abdullah University of Science and Technology; Arabia Saudita - Materia
-
Babesia bigemina
Variant antigen genes
Host-Parasite interaction - Nivel de accesibilidad
- acceso abierto
- Condiciones de uso
- https://creativecommons.org/licenses/by-nc/2.5/ar/
- Repositorio
.jpg)
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/33757
Ver los metadatos del registro completo
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The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interactionJackson, Andrew P.Otto, Thomas D.Darby, AlistairRamaprasad, AbhinayXia, DongEchaide, Ignacio EduardoFarber, Marisa DianaGahlot, SunaynaGamble, JohnGupta, DineshGupta, YaskJackson, LouiseMalandrin, LaurenceMalas, Tareq B.Moussa, EhabNair, MridulReid, Adam J.Sanders, MandySharma, JyotsnaTracey, AlanQuail, Mike A.Weir, WilliamWastling, Jonathan M.Hall, NeilWilladsen, PeterLingelbach, KlausShiels, BrianTait, AndyBerriman, MattAllred, David R.Pain, ArnabBabesia bigeminaVariant antigen genesHost-Parasite interactionhttps://purl.org/becyt/ford/4.3https://purl.org/becyt/ford/4Babesia spp. are tick-borne, intraerythrocytic hemoparasites that use antigenic variation to resist host immunity, through sequential modification of the parasite-derived variant erythrocyte surface antigen (VESA) expressed on the infected red blood cell surface. We identified the genomic processes driving antigenic diversity in genes encoding VESA (ves1) through comparative analysis within and between three Babesia species, (B. bigemina, B. divergens and B. bovis). Ves1 structure diverges rapidly after speciation, notably through the evolution of shortened forms (ves2) from 5´ ends of canonical ves1 genes. Phylogenetic analyses show that ves1 genes are transposed between loci routinely, whereas ves2 genes are not. Similarly, analysis of sequence mosaicism shows that recombination drives variation in ves1 sequences, but less so for ves2, indicating the adoption of different mechanisms for variation of the two families. Proteomic analysis of the B. bigemina PR isolate shows that two dominant VESA1 proteins are expressed in the population, whereas numerous VESA2 proteins are co-expressed, consistent with differential transcriptional regulation of each family. Hence, VESA2 proteins are abundant and previously unrecognized elements of Babesia biology, with evolutionary dynamics consistently different to those of VESA1, suggesting that their functions are distinct.Fil: Jackson, Andrew P.. University of Liverpool; Reino UnidoFil: Otto, Thomas D.. Wellcome Trust Sanger Institute; Reino UnidoFil: Darby, Alistair. University of Liverpool; Reino UnidoFil: Ramaprasad, Abhinay. King Abdullah University of Science and Technology; Arabia SauditaFil: Xia, Dong. University of Liverpool; Reino UnidoFil: Echaide, Ignacio Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Santa Fe. Estación Experimental Agropecuaria Rafaela; ArgentinaFil: Farber, Marisa Diana. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Gahlot, Sunayna. International Centre for Genetic Engineering and Biotechnology; IndiaFil: Gamble, John. Wellcome Trust Sanger Institute; Reino UnidoFil: Gupta, Dinesh. International Centre for Genetic Engineering and Biotechnology; IndiaFil: Gupta, Yask. International Centre for Genetic Engineering and Biotechnology; IndiaFil: Jackson, Louise. Biosecurity Sciences Laboratory. Department of Agriculture, Fisheries and Forestry; AustraliaFil: Malandrin, Laurence. Institut National de la Recherche Agronomique; Francia. Oniris. Research Unit Biology, Epidemiology and Risk Analysis in Animal Health; FranciaFil: Malas, Tareq B.. King Abdullah University of Science and Technology; Arabia SauditaFil: Moussa, Ehab. King Abdullah University of Science and Technology; Arabia SauditaFil: Nair, Mridul. King Abdullah University of Science and Technology; Arabia SauditaFil: Reid, Adam J.. Wellcome Trust Sanger Institute; Reino UnidoFil: Sanders, Mandy. Wellcome Trust Sanger Institute; Reino UnidoFil: Sharma, Jyotsna. Universitat Phillips; AlemaniaFil: Tracey, Alan. Wellcome Trust Sanger Institute; Reino UnidoFil: Quail, Mike A.. Wellcome Trust Sanger Institute; Reino UnidoFil: Weir, William. Universitat Phillips; AlemaniaFil: Wastling, Jonathan M.. University of Liverpool; Reino UnidoFil: Hall, Neil. University of Liverpool; Reino UnidoFil: Willadsen, Peter. Oniris. Research Unit Biology, Epidemiology and Risk Analysis in Animal Health; Francia. Institut National de la Recherche Agronomique; FranciaFil: Lingelbach, Klaus. Universitat Phillips; AlemaniaFil: Shiels, Brian. University of Glasgow; Reino UnidoFil: Tait, Andy. University of Glasgow; Reino UnidoFil: Berriman, Matt. Wellcome Trust Sanger Institute; Reino UnidoFil: Allred, David R.. University of Florida; Estados UnidosFil: Pain, Arnab. King Abdullah University of Science and Technology; Arabia SauditaOxford University Press2014-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/33757Jackson, Andrew P.; Otto, Thomas D.; Darby, Alistair; Ramaprasad, Abhinay; Xia, Dong; et al.; The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction; Oxford University Press; Nucleic Acids Research; 42; 11; 4-2014; 7113-71310305-10481362-4962CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/nar/article-lookup/doi/10.1093/nar/gku322info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4066756/info:eu-repo/semantics/altIdentifier/doi/10.1093/nar/gku322info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:16:41Zoai:ri.conicet.gov.ar:11336/33757instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:16:41.356CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse |
| dc.title.none.fl_str_mv |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| title |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| spellingShingle |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction Jackson, Andrew P. Babesia bigemina Variant antigen genes Host-Parasite interaction |
| title_short |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| title_full |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| title_fullStr |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| title_full_unstemmed |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| title_sort |
The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction |
| dc.creator.none.fl_str_mv |
Jackson, Andrew P. Otto, Thomas D. Darby, Alistair Ramaprasad, Abhinay Xia, Dong Echaide, Ignacio Eduardo Farber, Marisa Diana Gahlot, Sunayna Gamble, John Gupta, Dinesh Gupta, Yask Jackson, Louise Malandrin, Laurence Malas, Tareq B. Moussa, Ehab Nair, Mridul Reid, Adam J. Sanders, Mandy Sharma, Jyotsna Tracey, Alan Quail, Mike A. Weir, William Wastling, Jonathan M. Hall, Neil Willadsen, Peter Lingelbach, Klaus Shiels, Brian Tait, Andy Berriman, Matt Allred, David R. Pain, Arnab |
| author |
Jackson, Andrew P. |
| author_facet |
Jackson, Andrew P. Otto, Thomas D. Darby, Alistair Ramaprasad, Abhinay Xia, Dong Echaide, Ignacio Eduardo Farber, Marisa Diana Gahlot, Sunayna Gamble, John Gupta, Dinesh Gupta, Yask Jackson, Louise Malandrin, Laurence Malas, Tareq B. Moussa, Ehab Nair, Mridul Reid, Adam J. Sanders, Mandy Sharma, Jyotsna Tracey, Alan Quail, Mike A. Weir, William Wastling, Jonathan M. Hall, Neil Willadsen, Peter Lingelbach, Klaus Shiels, Brian Tait, Andy Berriman, Matt Allred, David R. Pain, Arnab |
| author_role |
author |
| author2 |
Otto, Thomas D. Darby, Alistair Ramaprasad, Abhinay Xia, Dong Echaide, Ignacio Eduardo Farber, Marisa Diana Gahlot, Sunayna Gamble, John Gupta, Dinesh Gupta, Yask Jackson, Louise Malandrin, Laurence Malas, Tareq B. Moussa, Ehab Nair, Mridul Reid, Adam J. Sanders, Mandy Sharma, Jyotsna Tracey, Alan Quail, Mike A. Weir, William Wastling, Jonathan M. Hall, Neil Willadsen, Peter Lingelbach, Klaus Shiels, Brian Tait, Andy Berriman, Matt Allred, David R. Pain, Arnab |
| author2_role |
author author author author author author author author author author author author author author author author author author author author author author author author author author author author author author |
| dc.subject.none.fl_str_mv |
Babesia bigemina Variant antigen genes Host-Parasite interaction |
| topic |
Babesia bigemina Variant antigen genes Host-Parasite interaction |
| purl_subject.fl_str_mv |
https://purl.org/becyt/ford/4.3 https://purl.org/becyt/ford/4 |
| dc.description.none.fl_txt_mv |
Babesia spp. are tick-borne, intraerythrocytic hemoparasites that use antigenic variation to resist host immunity, through sequential modification of the parasite-derived variant erythrocyte surface antigen (VESA) expressed on the infected red blood cell surface. We identified the genomic processes driving antigenic diversity in genes encoding VESA (ves1) through comparative analysis within and between three Babesia species, (B. bigemina, B. divergens and B. bovis). Ves1 structure diverges rapidly after speciation, notably through the evolution of shortened forms (ves2) from 5´ ends of canonical ves1 genes. Phylogenetic analyses show that ves1 genes are transposed between loci routinely, whereas ves2 genes are not. Similarly, analysis of sequence mosaicism shows that recombination drives variation in ves1 sequences, but less so for ves2, indicating the adoption of different mechanisms for variation of the two families. Proteomic analysis of the B. bigemina PR isolate shows that two dominant VESA1 proteins are expressed in the population, whereas numerous VESA2 proteins are co-expressed, consistent with differential transcriptional regulation of each family. Hence, VESA2 proteins are abundant and previously unrecognized elements of Babesia biology, with evolutionary dynamics consistently different to those of VESA1, suggesting that their functions are distinct. Fil: Jackson, Andrew P.. University of Liverpool; Reino Unido Fil: Otto, Thomas D.. Wellcome Trust Sanger Institute; Reino Unido Fil: Darby, Alistair. University of Liverpool; Reino Unido Fil: Ramaprasad, Abhinay. King Abdullah University of Science and Technology; Arabia Saudita Fil: Xia, Dong. University of Liverpool; Reino Unido Fil: Echaide, Ignacio Eduardo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Regional Santa Fe. Estación Experimental Agropecuaria Rafaela; Argentina Fil: Farber, Marisa Diana. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro Nacional de Investigaciones Agropecuarias; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Gahlot, Sunayna. International Centre for Genetic Engineering and Biotechnology; India Fil: Gamble, John. Wellcome Trust Sanger Institute; Reino Unido Fil: Gupta, Dinesh. International Centre for Genetic Engineering and Biotechnology; India Fil: Gupta, Yask. International Centre for Genetic Engineering and Biotechnology; India Fil: Jackson, Louise. Biosecurity Sciences Laboratory. Department of Agriculture, Fisheries and Forestry; Australia Fil: Malandrin, Laurence. Institut National de la Recherche Agronomique; Francia. Oniris. Research Unit Biology, Epidemiology and Risk Analysis in Animal Health; Francia Fil: Malas, Tareq B.. King Abdullah University of Science and Technology; Arabia Saudita Fil: Moussa, Ehab. King Abdullah University of Science and Technology; Arabia Saudita Fil: Nair, Mridul. King Abdullah University of Science and Technology; Arabia Saudita Fil: Reid, Adam J.. Wellcome Trust Sanger Institute; Reino Unido Fil: Sanders, Mandy. Wellcome Trust Sanger Institute; Reino Unido Fil: Sharma, Jyotsna. Universitat Phillips; Alemania Fil: Tracey, Alan. Wellcome Trust Sanger Institute; Reino Unido Fil: Quail, Mike A.. Wellcome Trust Sanger Institute; Reino Unido Fil: Weir, William. Universitat Phillips; Alemania Fil: Wastling, Jonathan M.. University of Liverpool; Reino Unido Fil: Hall, Neil. University of Liverpool; Reino Unido Fil: Willadsen, Peter. Oniris. Research Unit Biology, Epidemiology and Risk Analysis in Animal Health; Francia. Institut National de la Recherche Agronomique; Francia Fil: Lingelbach, Klaus. Universitat Phillips; Alemania Fil: Shiels, Brian. University of Glasgow; Reino Unido Fil: Tait, Andy. University of Glasgow; Reino Unido Fil: Berriman, Matt. Wellcome Trust Sanger Institute; Reino Unido Fil: Allred, David R.. University of Florida; Estados Unidos Fil: Pain, Arnab. King Abdullah University of Science and Technology; Arabia Saudita |
| description |
Babesia spp. are tick-borne, intraerythrocytic hemoparasites that use antigenic variation to resist host immunity, through sequential modification of the parasite-derived variant erythrocyte surface antigen (VESA) expressed on the infected red blood cell surface. We identified the genomic processes driving antigenic diversity in genes encoding VESA (ves1) through comparative analysis within and between three Babesia species, (B. bigemina, B. divergens and B. bovis). Ves1 structure diverges rapidly after speciation, notably through the evolution of shortened forms (ves2) from 5´ ends of canonical ves1 genes. Phylogenetic analyses show that ves1 genes are transposed between loci routinely, whereas ves2 genes are not. Similarly, analysis of sequence mosaicism shows that recombination drives variation in ves1 sequences, but less so for ves2, indicating the adoption of different mechanisms for variation of the two families. Proteomic analysis of the B. bigemina PR isolate shows that two dominant VESA1 proteins are expressed in the population, whereas numerous VESA2 proteins are co-expressed, consistent with differential transcriptional regulation of each family. Hence, VESA2 proteins are abundant and previously unrecognized elements of Babesia biology, with evolutionary dynamics consistently different to those of VESA1, suggesting that their functions are distinct. |
| publishDate |
2014 |
| dc.date.none.fl_str_mv |
2014-04 |
| dc.type.none.fl_str_mv |
info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://purl.org/coar/resource_type/c_6501 info:ar-repo/semantics/articulo |
| format |
article |
| status_str |
publishedVersion |
| dc.identifier.none.fl_str_mv |
http://hdl.handle.net/11336/33757 Jackson, Andrew P.; Otto, Thomas D.; Darby, Alistair; Ramaprasad, Abhinay; Xia, Dong; et al.; The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction; Oxford University Press; Nucleic Acids Research; 42; 11; 4-2014; 7113-7131 0305-1048 1362-4962 CONICET Digital CONICET |
| url |
http://hdl.handle.net/11336/33757 |
| identifier_str_mv |
Jackson, Andrew P.; Otto, Thomas D.; Darby, Alistair; Ramaprasad, Abhinay; Xia, Dong; et al.; The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction; Oxford University Press; Nucleic Acids Research; 42; 11; 4-2014; 7113-7131 0305-1048 1362-4962 CONICET Digital CONICET |
| dc.language.none.fl_str_mv |
eng |
| language |
eng |
| dc.relation.none.fl_str_mv |
info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/nar/article-lookup/doi/10.1093/nar/gku322 info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4066756/ info:eu-repo/semantics/altIdentifier/doi/10.1093/nar/gku322 |
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info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by-nc/2.5/ar/ |
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openAccess |
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https://creativecommons.org/licenses/by-nc/2.5/ar/ |
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application/pdf application/pdf application/pdf |
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Oxford University Press |
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Oxford University Press |
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Consejo Nacional de Investigaciones Científicas y Técnicas |
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CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas |
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dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar |
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