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Genome Integration and Reactivation of the Virophage Mavirus in the Marine Protozoan Cafeteria Roenbergensis

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Genome Integration and Reactivation of the Virophage Mavirus in the Marine Protozoan Cafeteria Roenbergensis bioRxiv preprint doi: https://doi.org/10.1101/068312; this version posted August 7, 2016. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Genome Integration and Reactivation of the Virophage Mavirus In the Marine Protozoan Cafeteria roenbergensis Matthias G. Fischer1* and Thomas Hackl1† 1Department of Biomolecular Mechanisms, Max Planck Institute for Medical Research, 69120 Heidelberg, Germany †Present address: Massachusetts Institute of Technology, 15 Vassar Street, Cambridge, MA 02139, USA Endogenous viral elements are increasingly found in eukaryotic genomes, yet little is known about their origins, dynamics, or function. Here, we provide a compelling example of a DNA virus that readily integrates into a eukaryotic genome where it acts as an inducible antiviral defense system. We found that the virophage mavirus, a parasite of the giant virus CroV, integrates at multiple sites within the nuclear genome of the marine heterotrophic nanoflagellate Cafeteria roenbergensis. The endogenous mavirus is structurally and genetically similar to the eukaryotic Maverick/Polinton DNA transposons. Provirophage genes are activated by superinfection with CroV, which leads to the production of infectious mavirus particles. While provirophage-carrying cells are not directly protected from lysis by CroV, release of reactivated virophage particles promotes survival of other host populations. Our results corroborate the connection between mavirus and Maverick/Polinton elements and suggest that provirophages can defend natural protist populations against infection by giant viruses. All viruses can potentially leave long-lasting One of the biggest surprises in recent imprints in cellular genomes. Some integrate into microbiological history was the discovery of protist- host genomes as part of their infection cycle; infecting giant viruses and their associated others lead exclusively lytic life styles, but can take virophages. Giant viruses are double-stranded (ds) advantage of rare stochastic events such as non- DNA viruses whose genomes can exceed 2000 homologous DNA recombination or by exploiting kilobase pairs (kbp)6,7. They are members of the helper functions from the cell and other viruses. To nucleocytoplasmic large DNA virus clade that date, endogenous viral elements (EVEs) for all includes the viral families Ascoviridae, major groups of viruses have been identified in Asfarviridae, Iridoviridae, Marseilleviridae, Mimi- eukaryotic genomes1. Whereas viral insertions are viridae, Phycodnaviridae, and Poxviridae8,9, as often disadvantageous for the host, there are well as the recently described pandoraviruses, fascinating examples where EVEs have evolved a pithoviruses, faustoviruses, and ‘Mollivirus host benefit, such as coopted retroviruses in sibericum’7,10–14. Many giant viruses reproduce in vertebrates2–4, or the symbiotic relationship of cytoplasmic virion factories (VFs), where polydnaviruses and parasitoid wasps5. However, transcription, DNA replication, and particle for the majority of non-retroviral EVEs, neither host assembly take place15. The presence of a viral function nor the circumstances of their transcription apparatus in these VFs permits the endogenization are known. Although most of the replication of so-called virophages, dsDNA viruses described EVEs are found in vertebrate genomes, with 15-30 kbp genomes that parasitize giant their occurrence is not restricted to multicellular viruses of the family Mimiviridae. Virophages are organisms. In particular the exogenous and strictly dependent for their replication on a endogenous viral spectrum of protists, which coinfecting giant virus16,17. The prediction that comprise the vast majority of eukaryotic diversity, virophages are transcriptional parasites of giant remains largely untapped. viruses is based on regulatory signals shared by __________ virophage and giant virus genes17–19. In addition, virophages encode their own morphogenesis and * Email: [email protected] DNA replication genes and appear to be 1 bioRxiv preprint doi: https://doi.org/10.1101/068312; this version posted August 7, 2016. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. autonomous for these processes. Coinfection with rve-INT. Despite the widespread occurrence of a giant virus and a virophage may result in integrase genes in virophages, it remains unclear decreased giant viral progeny and increased host under which conditions and how frequently these survival rates. viruses are able to integrate into eukaryotic Virophages are classified in the family genomes. Lavidaviridae20 with currently three members: the This motivated us to test the endogenization amoeba-infecting Sputnik virus and Zamilon potential of mavirus in its host C. roenbergensis. virus16,21, and the Maverick-related virus (mavirus). We show that mavirus readily integrates into the Mavirus possesses a 19,063 bp circular dsDNA nuclear genome of C. roenbergensis, where it is genome that is packaged inside a ≈75 nm wide vertically transmitted. We genetically characterized icosahedral capsid17. The cellular host for mavirus a host strain that carries more than eleven de novo is the heterotrophic nanoflagellate Cafeteria mavirus integrations and demonstrate close roenbergensis22, a bacterivorous protist that is structural similarity between the endogenous commonly found in marine environments and mavirus elements and MPEs. Our investigation reproduces by binary fission. The viral host for reveals an inducible model system to study the mavirus is Cafeteria roenbergensis virus (CroV), a integration and reactivation of a eukaryotic DNA ≈700 kbp dsDNA virus with a 300 nm large capsid virus. Furthermore, we show that provirophages that lyses its host within 24 hours post infection (h can act as a kin-based defense system against p.i.)23. The mavirus genome codes for 20 proteins, giant viruses in protists. seven of which have homologs among a group of mobile DNA elements called Mavericks or Results Polintons. Maverick/Polinton elements (MPEs) are present in Isolation of a mavirus-positive host strain various eukaryotic lineages and stand out from We devised a straight-forward infection experiment other DNA transposons due to their size (15-20 to test whether mavirus was able to integrate in kbp) and the viral nature of their genes24–26. All vivo into the nuclear genome of C. roenbergensis MPEs encode a retroviral integrase (rve-INT) and (Figure 1). For our experiments, we chose C. a protein-primed DNA polymerase B (pPolB); most roenbergensis strain E4-10 (originally misclassified elements also encode an FtsK-HerA-type genome as Bodo sp.) that was isolated in the early 1990s packaging adenosine triphosphatase (ATPase), an from Pacific waters off the coast of Oregon, USA33, adenovirus-like cysteine protease (PRO), and and which had proven to be a productive host for sporadically a superfamily 3 helicase (HEL). Two CroV and mavirus23. To ensure that the host strain additional conserved MPE genes were recently was genetically homogeneous, we performed identified as distant versions of the jelly-roll-fold single-cell dilutions and established clonal minor and major capsid protein genes that are also populations. This procedure was serially repeated encoded by virophages26. Whereas capsidless two more times and one of the resulting clonal MPEs likely spread as transposons, the capsid- strains was selected for further experiments encoding MPEs can be considered endogenous (Figure 1A). PCR testing of multiple mavirus target viruses (“polintoviruses”) and may in fact be the genes confirmed the absence of mavirus-specific most broadly distributed family of EVEs among sequences in this strain that we named E4-10P, eukaryotes27–29. Conversely, mavirus-like viro- being the parental strain for the study. The E4-10P phages can be viewed as the infectious form of strain was then either mock-infected with culture MPEs. Although the common evolutionary origin of medium or infected with CroV at a multiplicity of MPEs and virophages is apparent, the infection (MOI) of 0.01 and with mavirus at an MOI directionality of this process is a matter of of ≈1 (in contrast to CroV, no direct infectivity debate17,28,30. A central role in the virophage-MPE assay exists for mavirus and its MOIs are connection falls onto the integrases encoded by estimated from qPCR data). Under these virophages. Sputnik carries a tyrosine recom- conditions, mavirus inhibits CroV reproduction binase and can integrate into the genome of the sufficiently to prevent complete lysis of the cell giant Lentille virus31. MPEs, mavirus, as well as a population (Figure S1). We then screened the family of endogenous virophage-like elements surviving cells for host-integrated mavirus. After found in the alga Bigelowiella natans32 encode an the survivor cells had been pelleted and washed 2 bioRxiv preprint doi: https://doi.org/10.1101/068312; this version posted August 7, 2016. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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