eLife (Nov 2016)
Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
- Eileen P Hamilton,
- Aurélie Kapusta,
- Piroska E Huvos,
- Shelby L Bidwell,
- Nikhat Zafar,
- Haibao Tang,
- Michalis Hadjithomas,
- Vivek Krishnakumar,
- Jonathan H Badger,
- Elisabet V Caler,
- Carsten Russ,
- Qiandong Zeng,
- Lin Fan,
- Joshua Z Levin,
- Terrance Shea,
- Sarah K Young,
- Ryan Hegarty,
- Riza Daza,
- Sharvari Gujja,
- Jennifer R Wortman,
- Bruce W Birren,
- Chad Nusbaum,
- Jainy Thomas,
- Clayton M Carey,
- Ellen J Pritham,
- Cédric Feschotte,
- Tomoko Noto,
- Kazufumi Mochizuki,
- Romeo Papazyan,
- Sean D Taverna,
- Paul H Dear,
- Donna M Cassidy-Hanley,
- Jie Xiong,
- Wei Miao,
- Eduardo Orias,
- Robert S Coyne
Affiliations
- Eileen P Hamilton
- Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
- Aurélie Kapusta
- ORCiD
- Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
- Piroska E Huvos
- Biochemistry and Molecular Biology, Southern Illinois University, Carbondale, United States
- Shelby L Bidwell
- J. Craig Venter Institute, Rockville, United States
- Nikhat Zafar
- J. Craig Venter Institute, Rockville, United States
- Haibao Tang
- J. Craig Venter Institute, Rockville, United States
- Michalis Hadjithomas
- J. Craig Venter Institute, Rockville, United States
- Vivek Krishnakumar
- ORCiD
- J. Craig Venter Institute, Rockville, United States
- Jonathan H Badger
- J. Craig Venter Institute, Rockville, United States
- Elisabet V Caler
- J. Craig Venter Institute, Rockville, United States
- Carsten Russ
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Qiandong Zeng
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Lin Fan
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Joshua Z Levin
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Terrance Shea
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Sarah K Young
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Ryan Hegarty
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Riza Daza
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Sharvari Gujja
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Jennifer R Wortman
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Bruce W Birren
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Chad Nusbaum
- Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States
- Jainy Thomas
- Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
- Clayton M Carey
- Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
- Ellen J Pritham
- Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
- Cédric Feschotte
- Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States
- Tomoko Noto
- Institute of Molecular Biotechnology, Vienna, Austria
- Kazufumi Mochizuki
- ORCiD
- Institute of Molecular Biotechnology, Vienna, Austria
- Romeo Papazyan
- Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United States
- Sean D Taverna
- Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United States
- Paul H Dear
- MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
- Donna M Cassidy-Hanley
- Department of Microbiology and Immunology, Cornell University, Ithaca, United States
- Jie Xiong
- Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
- Wei Miao
- Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China
- Eduardo Orias
- Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States
- Robert S Coyne
- ORCiD
- J. Craig Venter Institute, Rockville, United States
- DOI
- https://doi.org/10.7554/eLife.19090
- Journal volume & issue
-
Vol. 5
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.
Keywords
- Tetrahymena thermophila
- chromosome breakage
- intermal eliminated sequence
- genome rearrangement
- transposable element
- centromere