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Genome analysis of three Pneumocystis species reveals adaptation mechanisms to life exclusively in mammalian hosts

Author

Listed:
  • Liang Ma

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Zehua Chen

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Da Wei Huang

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research
    Present address: Laboratory of Molecular Biology, National Cancer Institute, Bethesda, Maryland 20892, USA)

  • Geetha Kutty

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Mayumi Ishihara

    (Complex Carbohydrate Research Center, University of Georgia)

  • Honghui Wang

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Amr Abouelleil

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Lisa Bishop

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Emma Davey

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Rebecca Deng

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Xilong Deng

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Lin Fan

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Giovanna Fantoni

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Michael Fitzgerald

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Emile Gogineni

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Jonathan M. Goldberg

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology
    Present address: Department of Infectious and Immunological Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts 02115, USA)

  • Grace Handley

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Xiaojun Hu

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Charles Huber

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Xiaoli Jiao

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Kristine Jones

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Joshua Z. Levin

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Yueqin Liu

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Pendexter Macdonald

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Alexandre Melnikov

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Castle Raley

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Monica Sassi

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Brad T. Sherman

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Xiaohong Song

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Sean Sykes

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Bao Tran

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Laura Walsh

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Yun Xia

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

  • Jun Yang

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Sarah Young

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Qiandong Zeng

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Xin Zheng

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Robert Stephens

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Chad Nusbaum

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Bruce W. Birren

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Parastoo Azadi

    (Complex Carbohydrate Research Center, University of Georgia)

  • Richard A. Lempicki

    (Leidos BioMedical Research, Inc., Frederick National Laboratory for Cancer Research)

  • Christina A. Cuomo

    (Genome Sequencing and Analysis Program, Broad Institute of Harvard and Massachusetts Institute of Technology)

  • Joseph A. Kovacs

    (NIH Clinical Center, National Institutes of Health, Building 10, Room 2C145, 10 Center Drive, Bethesda, Maryland 20892, USA)

Abstract

Pneumocystis jirovecii is a major cause of life-threatening pneumonia in immunosuppressed patients including transplant recipients and those with HIV/AIDS, yet surprisingly little is known about the biology of this fungal pathogen. Here we report near complete genome assemblies for three Pneumocystis species that infect humans, rats and mice. Pneumocystis genomes are highly compact relative to other fungi, with substantial reductions of ribosomal RNA genes, transporters, transcription factors and many metabolic pathways, but contain expansions of surface proteins, especially a unique and complex surface glycoprotein superfamily, as well as proteases and RNA processing proteins. Unexpectedly, the key fungal cell wall components chitin and outer chain N-mannans are absent, based on genome content and experimental validation. Our findings suggest that Pneumocystis has developed unique mechanisms of adaptation to life exclusively in mammalian hosts, including dependence on the lungs for gas and nutrients and highly efficient strategies to escape both host innate and acquired immune defenses.

Suggested Citation

  • Liang Ma & Zehua Chen & Da Wei Huang & Geetha Kutty & Mayumi Ishihara & Honghui Wang & Amr Abouelleil & Lisa Bishop & Emma Davey & Rebecca Deng & Xilong Deng & Lin Fan & Giovanna Fantoni & Michael Fit, 2016. "Genome analysis of three Pneumocystis species reveals adaptation mechanisms to life exclusively in mammalian hosts," Nature Communications, Nature, vol. 7(1), pages 1-14, April.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms10740
    DOI: 10.1038/ncomms10740
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    Cited by:

    1. Caroline S. Meier & Marco Pagni & Sophie Richard & Konrad Mühlethaler & João M. G. C. F. Almeida & Gilles Nevez & Melanie T. Cushion & Enrique J. Calderón & Philippe M. Hauser, 2023. "Fungal antigenic variation using mosaicism and reassortment of subtelomeric genes’ repertoires," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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