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Endogenous virophages populate the genomes of a marine 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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  • ORCID record for Sarah Duponchel
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

Endogenous viral elements (EVEs) are frequently found in eukaryotic genomes, yet their integration dynamics and biological functions remain largely unknown. Unlike most other eukaryotic DNA viruses, the virophage mavirus integrates efficiently into the nuclear genome of its host, the marine heterotrophic flagellate Cafeteria burkhardae. Mavirus EVEs can reactivate upon superinfection with the lytic giant virus CroV and may act as an adaptive antiviral defense system, because mavirus increases host population survival during a coinfection with CroV. However, the prevalence of endogenous virophages in natural flagellate populations has not been explored. Here we report dozens of endogenous mavirus-like elements (EMALEs) in the nuclear genomes of four C. burkhardae strains. EMALEs were typically 20 kilobase pairs long and constituted 0.7% to 1.8% of each host genome. We analyzed 33 fully assembled EMALEs that fell into two main clusters and eight types based on GC-content, nucleotide similarity, and coding potential. Inter-strain comparison showed conservation of some EMALE insertion loci, whereas the majority of integration sites were unique to a given host strain. We also describe a group of tyrosine recombinase retrotransposons, some of which exhibited a strong preference for integration into EMALEs and represent yet another layer of parasitism in this microbial system. Our findings show that virophages are common, diverse, and dynamic genome components of the marine protist C. burkhardae, which implies important eco-evolutionary roles for these enigmatic viruses.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

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

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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 November 30, 2020.
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Endogenous virophages populate the genomes of a marine 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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Endogenous virophages populate the genomes of a marine 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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