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Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

View ORCID ProfileThomas Hackl, View ORCID ProfileSarah Duponchel, Karina Barenhoff, Alexa Weinmann, View ORCID ProfileMatthias G. Fischer
doi: https://doi.org/10.1101/2020.11.30.404863
Thomas Hackl
1Max Planck Institute for Medical Research, Department of Biomolecular Mechanisms, 69120 Heidelberg, Germany
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Sarah Duponchel
1Max Planck Institute for Medical Research, Department of Biomolecular Mechanisms, 69120 Heidelberg, Germany
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Karina Barenhoff
1Max Planck Institute for Medical Research, Department of Biomolecular Mechanisms, 69120 Heidelberg, Germany
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Alexa Weinmann
1Max Planck Institute for Medical Research, Department of Biomolecular Mechanisms, 69120 Heidelberg, Germany
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Matthias G. Fischer
1Max Planck Institute for Medical Research, Department of Biomolecular Mechanisms, 69120 Heidelberg, Germany
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  • ORCID record for Matthias G. Fischer
  • For correspondence: mfischer@mr.mpg.de
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Abstract

Virophages can parasitize giant DNA viruses and may provide adaptive anti-giant-virus defense in unicellular eukaryotes. Under laboratory conditions, the virophage mavirus integrates into the nuclear genome of the marine flagellate Cafeteria burkhardae and reactivates upon superinfection with the giant virus CroV. In natural systems, however, the prevalence and diversity of host-virophage associations has not been systematically explored. Here, we report dozens of integrated virophages in four globally sampled C. burkhardae strains that constitute up to 2% of their host genomes. These endogenous mavirus-like elements (EMALEs) separated into eight types based on GC-content, nucleotide similarity, and coding potential and carried diverse promoter motifs implicating interactions with different giant viruses. Between host strains, some EMALE insertion loci were conserved indicating ancient integration events, whereas the majority of insertion sites were unique to a given host strain suggesting that EMALEs are active and mobile. Furthermore, we uncovered a unique association between EMALEs and a group of tyrosine recombinase retrotransposons, revealing yet another layer of parasitism in this nested microbial system. Our findings show that virophages are widespread and dynamic in wild Cafeteria populations, supporting their potential role in antiviral defense in protists.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/thackl/cb-emales

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 13, 2021.
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Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate
Thomas Hackl, Sarah Duponchel, Karina Barenhoff, Alexa Weinmann, Matthias G. Fischer
bioRxiv 2020.11.30.404863; doi: https://doi.org/10.1101/2020.11.30.404863
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Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate
Thomas Hackl, Sarah Duponchel, Karina Barenhoff, Alexa Weinmann, Matthias G. Fischer
bioRxiv 2020.11.30.404863; doi: https://doi.org/10.1101/2020.11.30.404863

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