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

Hernan Lorenzi; Asis Khan; Michael S. Behnke; Sivaranjani Namasivayam; Lakshmipuram S. Swapna; Michalis Hadjithomas; Svetlana Karamycheva; Deborah Pinney; Brian P. Brunk; James W. Ajioka; Daniel Ajzenberg; John C. Boothroyd; Jon P. Boyle; Marie L. Dardé; Maria A. Diaz-Miranda; Jitender P. Dubey; Heather M. Fritz; Solange M. Gennari; Brian D. Gregory; Kami Kim; Jeroen P.J. Saeij; Chunlei Su; Michael W. White; Xing Quan Zhu; Daniel K. Howe; Benjamin M. Rosenthal; Michael E. Grigg; John Parkinson; Liang Liu; Jessica C. Kissinger; David S. Roos; L. David Sibley

doi:10.1038/ncomms10147

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

Hernan Lorenzi, Asis Khan, Michael S. Behnke, Sivaranjani Namasivayam, Lakshmipuram S. Swapna, Michalis Hadjithomas, Svetlana Karamycheva, Deborah Pinney, Brian P. Brunk, James W. Ajioka, Daniel Ajzenberg, John C. Boothroyd, Jon P. Boyle, Marie L. Dardé, Maria A. Diaz-Miranda, Jitender P. Dubey, Heather M. Fritz, Solange M. Gennari, Brian D. Gregory, Kami KimJeroen P.J. Saeij, Chunlei Su, Michael W. White, Xing Quan Zhu, Daniel K. Howe, Benjamin M. Rosenthal, Michael E. Grigg, John Parkinson, Liang Liu, Jessica C. Kissinger, David S. Roos, L. David Sibley

Research output: Contribution to journal › Article › peer-review

203 Scopus citations

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.

Original language	English
Article number	10147
Journal	Nature Communications
Volume	7
DOIs	https://doi.org/10.1038/ncomms10147
State	Published - Jan 7 2016

Bibliographical note

Funding Information:
Sequencing, assembly and annotation for the Tg and Hh genomes reported here were supported by the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Department of Health and Human Services under contract number HHSN272200900007C. Additional analyses were provided by community-based efforts and included support from NIH grants AI059176 and AI036629 (L.D.S.) and the Canadian Institutes for Health Research grant MOP 84556 (J.P.). Data for the Sn annotation was generously provided by M.E.G. and J.P. prior to publication and was supported by the Intramural Research Program of NIAID at the NIH (M.E.G.). Additional computing resources were provided by the SciNet HPC Consortium. We acknowledge ToxoDB (http://toxodb.org/) for providing a publically available repository for all genomic data described here and for assistance in coordinating this study. OrthoMCL and ToxoDB are supported in part with funds from the NIAID, NIH, and Department of Health and Human Services under contract HHSN272201400030C (D.S.R. & J.C.K.).

Funding Information:
Sequencing, assembly and annotation for the Tg and Hh genomes reported here were supported by the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Department of Health and Human Services under contract number HHSN272200900007C. Additional analyses were provided by community-based efforts and included support from NIH grants AI059176 and AI036629 (L.D.S.) and the Canadian Institutes for Health Research grant MOP 84556 (J.P.). Data for the Sn annotation was generously provided by M.E.G. and J.P. prior to publication and was supported by the Intramural Research Program of NIAID at the NIH (M.E.G.). Additional computing resources were provided by the SciNet HPC Consortium. We acknowledge ToxoDB (http://toxodb.org/) for providing a publically available repository for all genomic data described here and for assistance in coordinating this study. OrthoMCL and ToxoDB are supported in part with funds from the NIAID, NIH, and Department of Health and Human Services under contract HHSN272201400030C (D.S.R. & J.C.K.).

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

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10.1038/ncomms10147

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Lorenzi, H., Khan, A., Behnke, M. S., Namasivayam, S., Swapna, L. S., Hadjithomas, M., Karamycheva, S., Pinney, D., Brunk, B. P., Ajioka, J. W., Ajzenberg, D., Boothroyd, J. C., Boyle, J. P., Dardé, M. L., Diaz-Miranda, M. A., Dubey, J. P., Fritz, H. M., Gennari, S. M., Gregory, B. D., ... Sibley, L. D. (2016). Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes. Nature Communications, 7, Article 10147. https://doi.org/10.1038/ncomms10147

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title = "Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes",

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.",

author = "Hernan Lorenzi and Asis Khan and Behnke, {Michael S.} and Sivaranjani Namasivayam and Swapna, {Lakshmipuram S.} and Michalis Hadjithomas and Svetlana Karamycheva and Deborah Pinney and Brunk, {Brian P.} and Ajioka, {James W.} and Daniel Ajzenberg and Boothroyd, {John C.} and Boyle, {Jon P.} and Dard{\'e}, {Marie L.} and Diaz-Miranda, {Maria A.} and Dubey, {Jitender P.} and Fritz, {Heather M.} and Gennari, {Solange M.} and Gregory, {Brian D.} and Kami Kim and Saeij, {Jeroen P.J.} and Chunlei Su and White, {Michael W.} and Zhu, {Xing Quan} and Howe, {Daniel K.} and Rosenthal, {Benjamin M.} and Grigg, {Michael E.} and John Parkinson and Liang Liu and Kissinger, {Jessica C.} and Roos, {David S.} and Sibley, {L. David}",

note = "Funding Information: Sequencing, assembly and annotation for the Tg and Hh genomes reported here were supported by the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Department of Health and Human Services under contract number HHSN272200900007C. Additional analyses were provided by community-based efforts and included support from NIH grants AI059176 and AI036629 (L.D.S.) and the Canadian Institutes for Health Research grant MOP 84556 (J.P.). Data for the Sn annotation was generously provided by M.E.G. and J.P. prior to publication and was supported by the Intramural Research Program of NIAID at the NIH (M.E.G.). Additional computing resources were provided by the SciNet HPC Consortium. We acknowledge ToxoDB (http://toxodb.org/) for providing a publically available repository for all genomic data described here and for assistance in coordinating this study. OrthoMCL and ToxoDB are supported in part with funds from the NIAID, NIH, and Department of Health and Human Services under contract HHSN272201400030C (D.S.R. & J.C.K.). Funding Information: Sequencing, assembly and annotation for the Tg and Hh genomes reported here were supported by the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Department of Health and Human Services under contract number HHSN272200900007C. Additional analyses were provided by community-based efforts and included support from NIH grants AI059176 and AI036629 (L.D.S.) and the Canadian Institutes for Health Research grant MOP 84556 (J.P.). Data for the Sn annotation was generously provided by M.E.G. and J.P. prior to publication and was supported by the Intramural Research Program of NIAID at the NIH (M.E.G.). Additional computing resources were provided by the SciNet HPC Consortium. We acknowledge ToxoDB (http://toxodb.org/) for providing a publically available repository for all genomic data described here and for assistance in coordinating this study. OrthoMCL and ToxoDB are supported in part with funds from the NIAID, NIH, and Department of Health and Human Services under contract HHSN272201400030C (D.S.R. & J.C.K.).",

year = "2016",

month = jan,

day = "7",

doi = "10.1038/ncomms10147",

language = "English",

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Lorenzi, H, Khan, A, Behnke, MS, Namasivayam, S, Swapna, LS, Hadjithomas, M, Karamycheva, S, Pinney, D, Brunk, BP, Ajioka, JW, Ajzenberg, D, Boothroyd, JC, Boyle, JP, Dardé, ML, Diaz-Miranda, MA, Dubey, JP, Fritz, HM, Gennari, SM, Gregory, BD, Kim, K, Saeij, JPJ, Su, C, White, MW, Zhu, XQ, Howe, DK, Rosenthal, BM, Grigg, ME, Parkinson, J, Liu, L, Kissinger, JC, Roos, DS & Sibley, LD 2016, 'Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes', Nature Communications, vol. 7, 10147. https://doi.org/10.1038/ncomms10147

TY - JOUR

T1 - Local admixture of amplified and diversified secreted pathogenesis determinants shapes mosaic Toxoplasma gondii genomes

AU - Lorenzi, Hernan

AU - Khan, Asis

AU - Behnke, Michael S.

AU - Namasivayam, Sivaranjani

AU - Swapna, Lakshmipuram S.

AU - Hadjithomas, Michalis

AU - Karamycheva, Svetlana

AU - Pinney, Deborah

AU - Brunk, Brian P.

AU - Ajioka, James W.

AU - Ajzenberg, Daniel

AU - Boothroyd, John C.

AU - Boyle, Jon P.

AU - Dardé, Marie L.

AU - Diaz-Miranda, Maria A.

AU - Dubey, Jitender P.

AU - Fritz, Heather M.

AU - Gennari, Solange M.

AU - Gregory, Brian D.

AU - Kim, Kami

AU - Saeij, Jeroen P.J.

AU - Su, Chunlei

AU - White, Michael W.

AU - Zhu, Xing Quan

AU - Howe, Daniel K.

AU - Rosenthal, Benjamin M.

AU - Grigg, Michael E.

AU - Parkinson, John

AU - Liu, Liang

AU - Kissinger, Jessica C.

AU - Roos, David S.

AU - Sibley, L. David

N1 - Funding Information: Sequencing, assembly and annotation for the Tg and Hh genomes reported here were supported by the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Department of Health and Human Services under contract number HHSN272200900007C. Additional analyses were provided by community-based efforts and included support from NIH grants AI059176 and AI036629 (L.D.S.) and the Canadian Institutes for Health Research grant MOP 84556 (J.P.). Data for the Sn annotation was generously provided by M.E.G. and J.P. prior to publication and was supported by the Intramural Research Program of NIAID at the NIH (M.E.G.). Additional computing resources were provided by the SciNet HPC Consortium. We acknowledge ToxoDB (http://toxodb.org/) for providing a publically available repository for all genomic data described here and for assistance in coordinating this study. OrthoMCL and ToxoDB are supported in part with funds from the NIAID, NIH, and Department of Health and Human Services under contract HHSN272201400030C (D.S.R. & J.C.K.). Funding Information: Sequencing, assembly and annotation for the Tg and Hh genomes reported here were supported by the National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Department of Health and Human Services under contract number HHSN272200900007C. Additional analyses were provided by community-based efforts and included support from NIH grants AI059176 and AI036629 (L.D.S.) and the Canadian Institutes for Health Research grant MOP 84556 (J.P.). Data for the Sn annotation was generously provided by M.E.G. and J.P. prior to publication and was supported by the Intramural Research Program of NIAID at the NIH (M.E.G.). Additional computing resources were provided by the SciNet HPC Consortium. We acknowledge ToxoDB (http://toxodb.org/) for providing a publically available repository for all genomic data described here and for assistance in coordinating this study. OrthoMCL and ToxoDB are supported in part with funds from the NIAID, NIH, and Department of Health and Human Services under contract HHSN272201400030C (D.S.R. & J.C.K.).

PY - 2016/1/7

Y1 - 2016/1/7

N2 - 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.

AB - 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.

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UR - http://www.scopus.com/inward/citedby.url?scp=84954091677&partnerID=8YFLogxK

U2 - 10.1038/ncomms10147

DO - 10.1038/ncomms10147

M3 - Article

C2 - 26738725

AN - SCOPUS:84954091677

SN - 2041-1723

VL - 7

JO - Nature Communications

JF - Nature Communications

M1 - 10147

ER -

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

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