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

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 rela...

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Main Authors: 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
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/19090
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author 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
spellingShingle 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
Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
eLife
Tetrahymena thermophila
chromosome breakage
intermal eliminated sequence
genome rearrangement
transposable element
centromere
author_facet 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
author_sort Eileen P Hamilton
title Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
title_short Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
title_full Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
title_fullStr Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
title_full_unstemmed Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
title_sort structure of the germline genome of tetrahymena thermophila and relationship to the massively rearranged somatic genome
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2016-11-01
description 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.
topic Tetrahymena thermophila
chromosome breakage
intermal eliminated sequence
genome rearrangement
transposable element
centromere
url https://elifesciences.org/articles/19090
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spelling doaj-5b8a3b25eb90453aad49d3598e13d79e2021-05-05T00:43:14ZengeLife Sciences Publications LtdeLife2050-084X2016-11-01510.7554/eLife.19090Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genomeEileen P Hamilton0Aurélie Kapusta1https://orcid.org/0000-0002-4131-903XPiroska E Huvos2Shelby L Bidwell3Nikhat Zafar4Haibao Tang5Michalis Hadjithomas6Vivek Krishnakumar7https://orcid.org/0000-0002-5227-0200Jonathan H Badger8Elisabet V Caler9Carsten Russ10Qiandong Zeng11Lin Fan12Joshua Z Levin13Terrance Shea14Sarah K Young15Ryan Hegarty16Riza Daza17Sharvari Gujja18Jennifer R Wortman19Bruce W Birren20Chad Nusbaum21Jainy Thomas22Clayton M Carey23Ellen J Pritham24Cédric Feschotte25Tomoko Noto26Kazufumi Mochizuki27https://orcid.org/0000-0001-7987-9852Romeo Papazyan28Sean D Taverna29Paul H Dear30Donna M Cassidy-Hanley31Jie Xiong32Wei Miao33Eduardo Orias34Robert S Coyne35https://orcid.org/0000-0002-7693-3996Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United StatesDepartment of Human Genetics, University of Utah School of Medicine, Salt Lake City, United StatesBiochemistry and Molecular Biology, Southern Illinois University, Carbondale, United StatesJ. Craig Venter Institute, Rockville, United StatesJ. Craig Venter Institute, Rockville, United StatesJ. Craig Venter Institute, Rockville, United StatesJ. Craig Venter Institute, Rockville, United StatesJ. Craig Venter Institute, Rockville, United StatesJ. Craig Venter Institute, Rockville, United StatesJ. Craig Venter Institute, Rockville, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesEli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United StatesDepartment of Human Genetics, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Human Genetics, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Human Genetics, University of Utah School of Medicine, Salt Lake City, United StatesDepartment of Human Genetics, University of Utah School of Medicine, Salt Lake City, United StatesInstitute of Molecular Biotechnology, Vienna, AustriaInstitute of Molecular Biotechnology, Vienna, AustriaDepartment of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United StatesDepartment of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United StatesMRC Laboratory of Molecular Biology, Cambridge, United KingdomDepartment of Microbiology and Immunology, Cornell University, Ithaca, United StatesInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaDepartment of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United StatesJ. Craig Venter Institute, Rockville, United StatesThe 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.https://elifesciences.org/articles/19090Tetrahymena thermophilachromosome breakageintermal eliminated sequencegenome rearrangementtransposable elementcentromere