Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes

  1. Yi Feng
  2. Rafik Neme
  3. Leslie Y Beh
  4. Xiao Chen
  5. Jasper Braun
  6. Michael W Lu
  7. Laura F Landweber  Is a corresponding author
  1. Columbia University, United States
  2. Universidad del Norte, Colombia
  3. Pacific Biosciences, United States
  4. University of South Florida, United States

Abstract

Ciliates are microbial eukaryotes that undergo extensive programmed genome rearrangement, a natural genome editing process that converts long germline chromosomes into smaller gene-rich somatic chromosomes. Three well-studied ciliates include Oxytricha trifallax, Tetrahymena thermophila and Paramecium tetraurelia, but only the Oxytricha lineage has a massively scrambled genome, whose assembly during development requires hundreds of thousands of precise programmed DNA joining events, representing the most complex genome dynamics of any known organism. Here we study the emergence of such complex genomes by examining the origin and evolution of discontinuous and scrambled genes in the Oxytricha lineage. This study compares six genomes from three species, the germline and somatic genomes for Euplotes woodruffi, Tetmemena sp., and the model ciliate Oxytricha trifallax. To complement existing data, we sequenced, assembled and annotated the germline and somatic genomes of Euplotes woodruffi, which provides an outgroup, and the germline genome of Tetmemena sp.. We find that the germline genome of Tetmemena is as massively scrambled and interrupted as Oxytricha's : 13.6% of its gene loci require programmed translocations and/or inversions, with some genes requiring hundreds of precise gene editing events during development. This study revealed that the earlier-diverged spirotrich, E. woodruffi, also has a scrambled genome, but only roughly half as many loci (7.3%) are scrambled. Furthermore, its scrambled genes are less complex, together supporting the position of Euplotes as a possible evolutionary intermediate in this lineage, in the process of accumulating complex evolutionary genome rearrangements, all of which require extensive repair to assemble functional coding regions. Comparative analysis also reveals that scrambled loci are often associated with local duplications, supporting a gradual model for the origin of complex, scrambled genomes via many small events of DNA duplication and decay.

Data availability

Custom scripts are public on https://github.com/yifeng-evo/Oxytricha_Tetmemena_Euplotes. DNA-seq reads and genome assemblies are available at GenBank under Bioprojects PRJNA694964 (Tetmemena sp.) and PRJNA781979 (Euplotes woodruffi). Genbank accession numbers for genomes are JAJKFJ000000000 (Tetmemena sp. Micronucleus genome), JAJLLS000000000 (Euplotes woodruffi Micronucleus genome), and JAJLLT000000000 (Euplotes woodruffi Macronucleus genome).Three replicates of RNA-seq reads for vegetative cells are available at GenBank under accession numbers of SRR21815378, SRR21815379, SRR21815380 for E. woodruffi and SRR21817702, SRR21817703 and SRR21817704 for Tetmemena sp..MDSs annotations for three species are available at https://doi.org/10.5061/dryad.5dv41ns96 and https://knot.math.usf.edu/mds_ies_db/2022/downloads.html (please select species from the drop-down menu).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Yi Feng

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    No competing interests declared.
  2. Rafik Neme

    Department of Chemistry and Biology, Universidad del Norte, Barranquilla, Colombia
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8462-5291
  3. Leslie Y Beh

    Department of Biochemistry, Columbia University, New York, United States
    Competing interests
    Leslie Y Beh, The author is currently employed by Illumina.
  4. Xiao Chen

    Pacific Biosciences, Menlo Park, United States
    Competing interests
    Xiao Chen, employed by Pacific Biosciences.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1432-268X
  5. Jasper Braun

    Department of Mathematics and Statistics, University of South Florida, Tampa, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1250-4399
  6. Michael W Lu

    Department of Biochemistry, Columbia University, New York, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4926-8839
  7. Laura F Landweber

    Department of Biochemistry, Columbia University, New York, United States
    For correspondence
    Laura.Landweber@columbia.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7030-8540

Funding

National Institutes of Health (R35GM122555)

  • Yi Feng

National Science Foundation (DMS1764366)

  • Yi Feng

Pew Latin American Fellows Program (no)

  • Rafik Neme

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

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Biology Tübingen, Germany

Publication history

  1. Received: August 25, 2022
  2. Accepted: November 3, 2022
  3. Accepted Manuscript published: November 24, 2022 (version 1)

Copyright

© 2022, Feng et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Yi Feng
  2. Rafik Neme
  3. Leslie Y Beh
  4. Xiao Chen
  5. Jasper Braun
  6. Michael W Lu
  7. Laura F Landweber
(2022)
Comparative genomics reveals insight into the evolutionary origin of massively scrambled genomes
eLife 11:e82979.
https://doi.org/10.7554/eLife.82979
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