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

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 Fitzgerald, Emile Gogineni, Jonathan M. Goldberg, Grace Handley, Xiaojun Hu, Charles Huber, Xiaoli Jiao, Kristine Jones, Joshua Z. Levin, Yueqin Liu, Pendexter Macdonald, Alexandre Melnikov, Castle Raley, Monica Sassi, Brad T. Sherman, Xiaohong Song, Sean Sykes, Bao Tran, Laura Walsh, Yun Xia, Jun Yang, Sarah Young, Qiandong Zeng, Xin Zheng, Robert Stephens, Chad Nusbaum, Bruce W. Birren, Parastoo Azadi, Richard A. Lempicki, Christina A. Cuomo () and Joseph A. Kovacs ()
Additional contact information
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
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
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

Nature Communications, 2016, vol. 7, issue 1, 1-14

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms10740

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