Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome
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
-
Micronuclear Genome AssemblyPublicly available at NCBI Nucleotide (accession no: AFSS00000000).
-
Tetrahymena thermophila SB210 micronuclear genome sequencingPublicly available at NCBI BioProject (accession no: PRJNA51571).
-
Macronuclear Genome AssemblyPublicly available at NCBI Nucleotide (accession no: AAGF03000000).
-
Tetrahymena thermophila Transcriptome SequencingPublicly available at NCBI BioProject (accession no: PRJNA177770).
Article and author information
Author details
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
- Kathleen Collins, University of California, Berkeley, United States
Version history
- Received: June 24, 2016
- Accepted: November 14, 2016
- Accepted Manuscript published: November 28, 2016 (version 1)
- 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.
Metrics
-
- 6,282
- views
-
- 953
- downloads
-
- 127
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Chromosomes and Gene Expression
Tiny animals known as tardigrades use a combination of DNA repair machinery and a novel protein to mend their genome after intense ionizing radiation.
-
- Chromosomes and Gene Expression
Extrachromosomal DNA is a common cause of oncogene amplification in cancer. The non-chromosomal inheritance of ecDNA enables tumors to rapidly evolve, contributing to treatment resistance and poor outcome for patients. The transcriptional context in which ecDNAs arise and progress, including chromosomally-driven transcription, is incompletely understood. We examined gene expression patterns of 870 tumors of varied histological types, to identify transcriptional correlates of ecDNA. Here, we show that ecDNA-containing tumors impact four major biological processes. Specifically, ecDNA-containing tumors up-regulate DNA damage and repair, cell cycle control, and mitotic processes, but down-regulate global immune regulation pathways. Taken together, these results suggest profound alterations in gene regulation in ecDNA-containing tumors, shedding light on molecular processes that give rise to their development and progression.