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

Author:

Hamilton Eileen P1,Kapusta Aurélie2ORCID,Huvos Piroska E3,Bidwell Shelby L4,Zafar Nikhat4,Tang Haibao4,Hadjithomas Michalis4,Krishnakumar Vivek4ORCID,Badger Jonathan H4,Caler Elisabet V4,Russ Carsten5,Zeng Qiandong5,Fan Lin5,Levin Joshua Z5,Shea Terrance5,Young Sarah K5,Hegarty Ryan5,Daza Riza5,Gujja Sharvari5,Wortman Jennifer R5,Birren Bruce W5,Nusbaum Chad5,Thomas Jainy2,Carey Clayton M2,Pritham Ellen J2,Feschotte Cédric2,Noto Tomoko6,Mochizuki Kazufumi6ORCID,Papazyan Romeo7,Taverna Sean D7,Dear Paul H8,Cassidy-Hanley Donna M9,Xiong Jie10,Miao Wei10,Orias Eduardo1,Coyne Robert S4ORCID

Affiliation:

1. Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, United States

2. Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, United States

3. Biochemistry and Molecular Biology, Southern Illinois University, Carbondale, United States

4. J. Craig Venter Institute, Rockville, United States

5. Eli and Edythe L. Broad Institute of Harvard and MIT, Cambridge, United States

6. Institute of Molecular Biotechnology, Vienna, Austria

7. Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, United States

8. MRC Laboratory of Molecular Biology, Cambridge, United Kingdom

9. Department of Microbiology and Immunology, Cornell University, Ithaca, United States

10. Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 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.

Funder

National Institutes of Health

Natural Science Foundation of Hubei Province

National Science Foundation

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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