Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes

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Abstract

Toxoplasma gondii is among the most prevalent parasites worldwide, infecting many wild and domestic animals and causing zoonotic infections in humans. T. gondii differs substantially in its broad distribution from closely related parasites that typically have narrow, specialized host ranges. To elucidate the genetic basis for these differences, we compared the genomes of 62 globally distributed T. gondii isolates to several closely related coccidian parasites. Our findings reveal that tandem amplification and diversification of secretory pathogenesis determinants is the primary feature that distinguishes the closely related genomes of these biologically diverse parasites. We further show that the unusual population structure of T. gondii is characterized by clade-specific inheritance of large conserved haploblocks that are significantly enriched in tandemly clustered secretory pathogenesis determinants. The shared inheritance of these conserved haploblocks, which show a different ancestry than the genome as a whole, may thus influence transmission, host range and pathogenicity.

Abstract

Toxoplasma gondii is a parasite that causes zoonotic infections in humans. Here, the authors identify tandem amplification and diversification of secretory pathogenesis determinants in the T. gondii genome and show that clade-specific inheritance of conserved haploblocks enriched for these determinants shapes population structure.

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Author and article information

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group

ISSN (Electronic): 2041-1723

Publication date (Electronic): 07 January 2016

Publication date Collection: 2016

Volume: 7

Electronic Location Identifier: 10147

Affiliations

[1 ]Department of Infectious Diseases, The J. Craig Venter Institute, 9704 Medical Center Drive , Rockville, Maryland 20850, USA

[2 ]Department of Molecular Microbiology, Washington University School of Medicine , 660 S. Euclid Avenue, St Louis, Missouri 63130, USA

[3 ]Laboratory of Parasitic Diseases, NIAID, National Institutes of Health , Bethesda, Maryland 20892, USA

[4 ]Pathobiological Sciences, School of Veterinary Medicine, Louisiana State University , Baton Rougea Louisian 70803, USA

[5 ]Department of Genetics, University of Georgia , Athens, Georgia 30602, USA

[6 ]Center for Tropical and Emerging Global Diseases, University of Georgia , Athens Georgia 30602, USA

[7 ]Program in Molecular Structure and Function, Hospital for Sick Children , Toronto, Ontario, Canada M5G 1L7

[8 ]Departments of Biochemistry and Molecular Genetics, University of Toronto , Toronto, Ontario, Canada M5S 1A8

[9 ]Department of Biology, University of Pennsylvania , Philadelphia, Pennsylvania 19104, USA

[10 ]Department of Pathology, University of Cambridge , Cambridge CB2 1QP, UK

[11 ]Biological Resource Center for Toxoplasma, INSERM, University Limoges, CHU Limoges, UMR_S 1094, Tropical Neuroepidemiology, Institute of Neuroepidemiology and Tropical Neurology , Limoges 87025, France

[12 ]Department of Microbiology and Immunology, Stanford School of Medicine , Stanford, California 94305, USA

[13 ]Department of Biological Sciences, Dietrich School of Arts and Sciences, University of Pittsburgh , Pittsburgh, Pennsylvania 15260, USA

[14 ]Animal Parasitic Diseases Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, USDA , Beltsville, Maryland 20705, USA

[15 ]Department of Veterinary Pathology and Microbiology, Washington State University, College of Veterinary Medicine , Pullman, Washington 99164, USA

[16 ]Department of Preventive Veterinary Medicine and Animal Health, Faculty of Veterinary Medicine, University of São Paulo , São Paulo, SP CEP 05598-270, Brazil

[17 ]Departments of Medicine, Pathology, and Microbiology and Immunology, Albert Einstein College of Medicine , Bronx, New York 10461, USA

[18 ]Department of Pathology, Microbiology & Immunology, University of California , David, California 95616, USA

[19 ]Department of Microbiology, University of Tennessee , Knoxville, Tennessee 37996, USA

[20 ]Departments of Molecular Medicine and Global Health, Florida Center for Drug Discovery and Development (CDDI), University of South Florida , 3720 Spectrum Boulevard, Suite 304, Tampa, Florida 33612, USA

[21 ]State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences , Lanzhou, Gansu Province 730046, China

[22 ]Department of Veterinary Science, University of Kentucky , Lexington, Kentucky 40546, USA

[23 ]Department of Statistics, University of Georgia , Athens Georgia 30602, USA

[24 ]Institute of Bioinformatics, University of Georgia , Athens, Georgia 30602, USA

Author notes

[a ] hlorenzi@ 123456jcvi.org

[b ] sibley@ 123456wustl.edu

[*]

These authors contributed equally to this work.

[†]

Present address: Prokaryotic Super Program, DOE Joint Genome Institute, Walnut Creek, California 94598, USA.

Author information

Svetlana Karamycheva http://orcid.org/0000-0001-9653-8910

Article

Publisher Item ID: ncomms10147

DOI: 10.1038/ncomms10147

PMC ID: 4729833

PubMed ID: 26738725

SO-VID: cb45f690-a93e-4087-ac0b-4dba23f6c568

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History

Date received : 21 January 2015

Date accepted : 09 November 2015

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Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes

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G3: Genes|Genomes|Genetics

Most cited references 42

Comparison of phylogenetic trees

The genome of the African trypanosome Trypanosoma brucei.

Fast algorithms for large-scale genome alignment and comparison.

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