Comparative genomics of the apicomplexan parasites Toxoplasma gondii and neospora caninum: Coccidia differing in host range and transmission strategy

Handle URI:
http://hdl.handle.net/10754/325344
Title:
Comparative genomics of the apicomplexan parasites Toxoplasma gondii and neospora caninum: Coccidia differing in host range and transmission strategy
Authors:
Reid, Adam James; Vermont, Sarah J.; Cotton, James A.; Harris, David; Hill-Cawthorne, Grant A. ( 0000-0002-3828-5473 ) ; Könen-Waisman, Stephanie; Latham, Sophia M.; Mourier, Tobias; Norton, Rebecca; Quail, Michael A.; Sanders, Mandy; Shanmugam, Dhanasekaran; Sohal, Amandeep; Wasmuth, James D.; Brunk, Brian; Grigg, Michael E.; Howard, Jonathan C.; Parkinson, John; Roos, David S.; Trees, Alexander J.; Berriman, Matthew; Pain, Arnab ( 0000-0002-1755-2819 ) ; Wastling, Jonathan M.
Abstract:
Toxoplasma gondii is a zoonotic protozoan parasite which infects nearly one third of the human population and is found in an extraordinary range of vertebrate hosts. Its epidemiology depends heavily on horizontal transmission, especially between rodents and its definitive host, the cat. Neospora caninum is a recently discovered close relative of Toxoplasma, whose definitive host is the dog. Both species are tissue-dwelling Coccidia and members of the phylum Apicomplexa; they share many common features, but Neospora neither infects humans nor shares the same wide host range as Toxoplasma, rather it shows a striking preference for highly efficient vertical transmission in cattle. These species therefore provide a remarkable opportunity to investigate mechanisms of host restriction, transmission strategies, virulence and zoonotic potential. We sequenced the genome of N. caninum and transcriptomes of the invasive stage of both species, undertaking an extensive comparative genomics and transcriptomics analysis. We estimate that these organisms diverged from their common ancestor around 28 million years ago and find that both genomes and gene expression are remarkably conserved. However, in N. caninum we identified an unexpected expansion of surface antigen gene families and the divergence of secreted virulence factors, including rhoptry kinases. Specifically we show that the rhoptry kinase ROP18 is pseudogenised in N. caninum and that, as a possible consequence, Neospora is unable to phosphorylate host immunity-related GTPases, as Toxoplasma does. This defense strategy is thought to be key to virulence in Toxoplasma. We conclude that the ecological niches occupied by these species are influenced by a relatively small number of gene products which operate at the host-parasite interface and that the dominance of vertical transmission in N. caninum may be associated with the evolution of reduced virulence in this species.
KAUST Department:
Biological and Environmental Sciences and Engineering (BESE) Division; Bioscience Program; Computational Bioscience Research Center (CBRC)
Citation:
Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, et al. (2012) Comparative Genomics of the Apicomplexan Parasites Toxoplasma gondii and Neospora caninum: Coccidia Differing in Host Range and Transmission Strategy. PLoS Pathog 8: e1002567. doi:10.1371/journal.ppat.1002567.
Publisher:
Public Library of Science (PLoS)
Journal:
PLoS Pathogens
Issue Date:
22-Mar-2012
DOI:
10.1371/journal.ppat.1002567
PubMed ID:
22457617
PubMed Central ID:
PMC3310773
Type:
Article
ISSN:
15537366
Appears in Collections:
Articles; Bioscience Program; Computational Bioscience Research Center (CBRC); Biological and Environmental Sciences and Engineering (BESE) Division

Full metadata record

DC FieldValue Language
dc.contributor.authorReid, Adam Jamesen
dc.contributor.authorVermont, Sarah J.en
dc.contributor.authorCotton, James A.en
dc.contributor.authorHarris, Daviden
dc.contributor.authorHill-Cawthorne, Grant A.en
dc.contributor.authorKönen-Waisman, Stephanieen
dc.contributor.authorLatham, Sophia M.en
dc.contributor.authorMourier, Tobiasen
dc.contributor.authorNorton, Rebeccaen
dc.contributor.authorQuail, Michael A.en
dc.contributor.authorSanders, Mandyen
dc.contributor.authorShanmugam, Dhanasekaranen
dc.contributor.authorSohal, Amandeepen
dc.contributor.authorWasmuth, James D.en
dc.contributor.authorBrunk, Brianen
dc.contributor.authorGrigg, Michael E.en
dc.contributor.authorHoward, Jonathan C.en
dc.contributor.authorParkinson, Johnen
dc.contributor.authorRoos, David S.en
dc.contributor.authorTrees, Alexander J.en
dc.contributor.authorBerriman, Matthewen
dc.contributor.authorPain, Arnaben
dc.contributor.authorWastling, Jonathan M.en
dc.date.accessioned2014-08-27T09:48:20Z-
dc.date.available2014-08-27T09:48:20Z-
dc.date.issued2012-03-22en
dc.identifier.citationReid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, et al. (2012) Comparative Genomics of the Apicomplexan Parasites Toxoplasma gondii and Neospora caninum: Coccidia Differing in Host Range and Transmission Strategy. PLoS Pathog 8: e1002567. doi:10.1371/journal.ppat.1002567.en
dc.identifier.issn15537366en
dc.identifier.pmid22457617en
dc.identifier.doi10.1371/journal.ppat.1002567en
dc.identifier.urihttp://hdl.handle.net/10754/325344en
dc.description.abstractToxoplasma gondii is a zoonotic protozoan parasite which infects nearly one third of the human population and is found in an extraordinary range of vertebrate hosts. Its epidemiology depends heavily on horizontal transmission, especially between rodents and its definitive host, the cat. Neospora caninum is a recently discovered close relative of Toxoplasma, whose definitive host is the dog. Both species are tissue-dwelling Coccidia and members of the phylum Apicomplexa; they share many common features, but Neospora neither infects humans nor shares the same wide host range as Toxoplasma, rather it shows a striking preference for highly efficient vertical transmission in cattle. These species therefore provide a remarkable opportunity to investigate mechanisms of host restriction, transmission strategies, virulence and zoonotic potential. We sequenced the genome of N. caninum and transcriptomes of the invasive stage of both species, undertaking an extensive comparative genomics and transcriptomics analysis. We estimate that these organisms diverged from their common ancestor around 28 million years ago and find that both genomes and gene expression are remarkably conserved. However, in N. caninum we identified an unexpected expansion of surface antigen gene families and the divergence of secreted virulence factors, including rhoptry kinases. Specifically we show that the rhoptry kinase ROP18 is pseudogenised in N. caninum and that, as a possible consequence, Neospora is unable to phosphorylate host immunity-related GTPases, as Toxoplasma does. This defense strategy is thought to be key to virulence in Toxoplasma. We conclude that the ecological niches occupied by these species are influenced by a relatively small number of gene products which operate at the host-parasite interface and that the dominance of vertical transmission in N. caninum may be associated with the evolution of reduced virulence in this species.en
dc.language.isoenen
dc.publisherPublic Library of Science (PLoS)en
dc.rightsThis is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.en
dc.rightsArchived with thanks to PLoS Pathogensen
dc.subjectmembrane antigenen
dc.subjectconservation geneticsen
dc.subjectgene expressionen
dc.subjectgene sequenceen
dc.subjectgenetic transcriptionen
dc.subjectgenomeen
dc.subjectNeospora caninumen
dc.subjectparasite virulenceen
dc.subjectphosphorylationen
dc.subjectsequence analysisen
dc.subjectspecies differenceen
dc.subjectToxoplasma gondiien
dc.subjectcoccidiosisen
dc.subjectcomparative genomic hybridizationen
dc.subjectcomparative studyen
dc.subjectdisease transmissionen
dc.subjectgene expression regulationen
dc.subjectgeneticsen
dc.subjectgenomicsen
dc.subjecthost parasite interactionen
dc.subjectNeosporaen
dc.subjectparasitologyen
dc.subjectpathogenicityen
dc.subjectphysiologyen
dc.subjectToxoplasmaen
dc.subjecttoxoplasmosisen
dc.subjectvertical transmissionen
dc.subjectvirulenceen
dc.subjectzoonosisen
dc.subjectApicomplexaen
dc.subjectBosen
dc.subjectCanis familiarisen
dc.subjectCoccidiaen
dc.subjectNeosporaen
dc.subjectNeospora caninumen
dc.subjectProtozoaen
dc.subjectRodentiaen
dc.subjectToxoplasmaen
dc.subjectToxoplasma gondiien
dc.subjectVertebrataen
dc.subjectCoccidiosisen
dc.subjectComparative Genomic Hybridizationen
dc.subjectGene Expression Regulationen
dc.subjectGenomicsen
dc.subjectHost-Parasite Interactionsen
dc.subjectInfectious Disease Transmission, Verticalen
dc.subjectNeosporaen
dc.subjectToxoplasmaen
dc.subjectToxoplasmosisen
dc.subjectVirulenceen
dc.subjectZoonosesen
dc.titleComparative genomics of the apicomplexan parasites Toxoplasma gondii and neospora caninum: Coccidia differing in host range and transmission strategyen
dc.typeArticleen
dc.contributor.departmentBiological and Environmental Sciences and Engineering (BESE) Divisionen
dc.contributor.departmentBioscience Programen
dc.contributor.departmentComputational Bioscience Research Center (CBRC)en
dc.identifier.journalPLoS Pathogensen
dc.identifier.pmcidPMC3310773en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionWellcome Trust Sanger Institute, Hinxton, Cambridgshire, United Kingdomen
dc.contributor.institutionInstitute of Infection and Global Health and School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, Liverpool, Merseyside, United Kingdomen
dc.contributor.institutionInstitute for Genetics, University of Cologne, Cologne, North Rhine-Westphalia, Germanyen
dc.contributor.institutionCentre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmarken
dc.contributor.institutionDepartment of Biology, University of Pennsylvania, Philadelphia, PA, United Statesen
dc.contributor.institutionProgram in Molecular Structure and Function, Hospital for Sick Children and Departments of Biochemistry and Molecular Genetics, University of Toronto, Toronto, ON, Canadaen
dc.contributor.institutionLaboratory of Parasitic Diseases, National Institutes of Health, National Institute of Allergy and Infectious Diseases (NIAID), Bethesda, MD, United Statesen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorHill-Cawthorne, Grant A.en
kaust.authorPain, Arnaben
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