Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome

  1. Eileen P Hamilton
  2. Aurélie Kapusta
  3. Piroska E Huvos
  4. Shelby L Bidwell
  5. Nikhat Zafar
  6. Haibao Tang
  7. Michalis Hadjithomas
  8. Vivek Krishnakumar
  9. Jonathan H Badger
  10. Elisabet V Caler
  11. Carsten Russ
  12. Qiandong Zeng
  13. Lin Fan
  14. Joshua Z Levin
  15. Terrance Shea
  16. Sarah K Young
  17. Ryan Hegarty
  18. Riza Daza
  19. Sharvari Gujja
  20. Jennifer R Wortman
  21. Bruce W Birren
  22. Chad Nusbaum
  23. Jainy Thomas
  24. Clayton M Carey
  25. Ellen J Pritham
  26. Cédric Feschotte
  27. Tomoko Noto
  28. Kazufumi Mochizuki
  29. Romeo Papazyan
  30. Sean D Taverna
  31. Paul H Dear
  32. Donna M Cassidy-Hanley
  33. Jie Xiong
  34. Wei Miao
  35. Eduardo Orias
  36. Robert S Coyne  Is a corresponding author
  1. University of California, Santa Barbara, United States
  2. University of Utah School of Medicine, United States
  3. Southern Illinois University, United States
  4. J. Craig Venter Institute, United States
  5. Eli and Edythe L. Broad Institute of Harvard and MIT, United States
  6. Broad Institute, United States
  7. Institute of Molecular Biotechnology, Austria
  8. The Johns Hopkins University School of Medicine, United States
  9. MRC Laboratory of Molecular Biology, United Kingdom
  10. Cornell University, United States
  11. Chinese Academy of Sciences, China

Abstract

The germline genome of the binucleated ciliate Tetrahymena thermophila undergoes programmed chromosome breakage and massive DNA elimination to generate the somatic genome. Here we present a complete sequence assembly of the germline genome and analyze multiple features of its structure and its relationship to the somatic genome, shedding light on the mechanisms of genome rearrangement as well as the evolutionary history of this remarkable germline/soma differentiation. Our results strengthen the notion that a complex, dynamic, and ongoing interplay between mobile DNA elements and the host genome have shaped Tetrahymena chromosome structure, locally and globally. Non-standard outcomes of rearrangement events, including the generation of short-lived somatic chromosomes and excision of DNA interrupting protein-coding regions, may represent novel forms of developmental gene regulation. We also compare Tetrahymena's germline/soma differentiation to that of other characterized ciliates, illustrating the wide diversity of adaptations that have occurred within this phylum.

Data availability

The following data sets were generated

Article and author information

Author details

  1. Eileen P Hamilton

    Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Aurélie Kapusta

    Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Piroska E Huvos

    Department of Medical Biochemistry, Southern Illinois University, Carbondale, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Shelby L Bidwell

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Nikhat Zafar

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Haibao Tang

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Michalis Hadjithomas

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Vivek Krishnakumar

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5227-0200
  9. Jonathan H Badger

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Elisabet V Caler

    J. Craig Venter Institute, Rockville, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Carsten Russ

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Qiandong Zeng

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Lin Fan

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Joshua Z Levin

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Terrance Shea

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Sarah K Young

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Ryan Hegarty

    Genomics Platform, Broad Institute, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. Riza Daza

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  19. Sharvari Gujja

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Jennifer R Wortman

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  21. Bruce W Birren

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  22. Chad Nusbaum

    Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  23. Jainy Thomas

    Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  24. Clayton M Carey

    Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  25. Ellen J Pritham

    Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  26. Cédric Feschotte

    Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  27. Tomoko Noto

    Institute of Molecular Biotechnology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  28. Kazufumi Mochizuki

    Institute of Molecular Biotechnology, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7987-9852
  29. Romeo Papazyan

    Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  30. Sean D Taverna

    Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  31. Paul H Dear

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  32. Donna M Cassidy-Hanley

    Department of Microbiology and Immunology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  33. Jie Xiong

    Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  34. Wei Miao

    Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  35. Eduardo Orias

    Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    The authors declare that no competing interests exist.
  36. Robert S Coyne

    J. Craig Venter Institute, Rockville, United States
    For correspondence
    rcoyne@jcvi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7693-3996

Funding

National Human Genome Research Institute (U54 HG003067)

  • Chad Nusbaum

National Science Foundation (MCB-1158346)

  • Robert S Coyne

Natural Science Foundation of Hubei Province (31525021)

  • Wei Miao

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Kathleen Collins, University of California, Berkeley, United States

Version history

  1. Received: June 24, 2016
  2. Accepted: November 14, 2016
  3. Accepted Manuscript published: November 28, 2016 (version 1)
  4. Version of Record published: December 23, 2016 (version 2)

Copyright

This 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.

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  1. Eileen P Hamilton
  2. Aurélie Kapusta
  3. Piroska E Huvos
  4. Shelby L Bidwell
  5. Nikhat Zafar
  6. Haibao Tang
  7. Michalis Hadjithomas
  8. Vivek Krishnakumar
  9. Jonathan H Badger
  10. Elisabet V Caler
  11. Carsten Russ
  12. Qiandong Zeng
  13. Lin Fan
  14. Joshua Z Levin
  15. Terrance Shea
  16. Sarah K Young
  17. Ryan Hegarty
  18. Riza Daza
  19. Sharvari Gujja
  20. Jennifer R Wortman
  21. Bruce W Birren
  22. Chad Nusbaum
  23. Jainy Thomas
  24. Clayton M Carey
  25. Ellen J Pritham
  26. Cédric Feschotte
  27. Tomoko Noto
  28. Kazufumi Mochizuki
  29. Romeo Papazyan
  30. Sean D Taverna
  31. Paul H Dear
  32. Donna M Cassidy-Hanley
  33. Jie Xiong
  34. Wei Miao
  35. Eduardo Orias
  36. Robert S Coyne
(2016)
Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
eLife 5:e19090.
https://doi.org/10.7554/eLife.19090

Share this article

https://doi.org/10.7554/eLife.19090

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