Paleovirology of the DNA viruses of eukaryotes

Barreat, Jose Gabriel Nino

doi:10.1016/j.tim.2021.07.004

Cited by 22 publications

(15 citation statements)

References 102 publications

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“…S2 , Supplementary Material online). Although noteworthy, this result agrees with the growing evidence for multiple HGT events between these large viruses and a variety of organisms (reviewed in Barreat and Katzourakis [2021] ).…”

Section: Resultssupporting

confidence: 90%

Pif1 Helicases and the Evidence for a Prokaryotic Origin of Helitrons

Heringer

Kuhn

2021

Molecular Biology and Evolution

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Helitrons are the only group of rolling-circle transposons that encode a transposase with a helicase domain (Hel), which belongs to the Pif1 family. Because Pif1 helicases are important components of eukaryotic genomes, it has been suggested that Hel domains probably originated after a host eukaryotic Pif1 gene was captured by a Helitron ancestor. However, the few analyses exploring the evolution of Helitron transposases (RepHel) have focused on its Rep domain, which is also present in other mobile genetic elements. Here, we used phylogenetic and non-metric multidimensional scaling analyses to investigate the relationship between Hel domains and Pif1-like helicases from a variety of organisms. Our results reveal that Hel domains are only distantly related to genomic helicases from eukaryotes and prokaryotes, and thus are unlikely to have originated from a captured Pif1 gene. Based on this evidence, and on recent studies indicating that Rep domains are more closely related to rolling-circle plasmids and phages, we suggest that Helitrons are descendants of a RepHel-encoding prokaryotic plasmid element that invaded eukaryotic genomes before the radiation of its major groups. We discuss how a Pif1-like helicase domain might have favored the transposition of Helitrons in eukaryotes beyond simply unwinding DNA intermediates. Finally, we demonstrate that some examples in the literature describing genomic helicases from eukaryotes actually consist of Hel domains from Helitrons, a finding that underscores how transposons can hamper the analysis of eukaryotic genes. This investigation also revealed that two groups of land plants appear to have lost genomic Pif1 helicases independently.

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Section: Resultssupporting

confidence: 90%

Pif1 Helicases and the Evidence for a Prokaryotic Origin of Helitrons

Heringer

Kuhn

2021

Molecular Biology and Evolution

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“…Given that multiple mavirus genome integrations per host cell can be observed within a period of days ( Fischer and Hackl, 2016 ) and that virophage integration rates under natural infection conditions are likely to fall within similar timescales, we hypothesize that the majority of EMALE loss may occur before pseudogenization and degradation can take place. EMALEs would thus have relatively short residence times in the unicellular Cafeteria compared to germline EVEs of multicellular eukaryotes ( Barreat and Katzourakis, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Hackl

Duponchel

Barenhoff

et al. 2021

eLife

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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.

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“…One promising application is paleovirology: Few Mesozoic and no Paleozoic viral fossils have been found so far ( Barreat and Katzourakis, 2022 ). If Gypsy-like elements (Metaviridae) or Polintons are counted as viruses, Paleozoic fossils predating ∼350 million years are found here ( table 4 ).…”

Section: Resultsmentioning

confidence: 99%

“…The boundary between TEs and viruses is blurry, and an entire field, paleovirology, is mainly based on viral insertion fossils in eukaryote genomes ( Barreat and Katzourakis, 2022 ). The oldest viral fossils found so far seem to be Mesozoic ( Suh et al 2014 ; Barreat and Katzourakis, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

Paleozoic Protein Fossils Illuminate the Evolution of Vertebrate Genomes and Transposable Elements

Frith

2022

Molecular Biology and Evolution

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Genomes hold a treasure trove of protein fossils: fragments of formerly protein-coding DNA, which mainly come from transposable elements (TEs) or host genes. These fossils reveal ancient evolution of TEs and genomes, and many fossils have been exapted to perform diverse functions important for the host’s fitness. However, old and highly-degraded fossils are hard to identify, standard methods (e.g. BLAST) are not optimized for this task, and few Paleozoic protein fossils have been found. Here, a recently optimized method is used to find protein fossils in vertebrate genomes. It finds Paleozoic fossils predating the amphibian/amniote divergence from most major TE categories, including virus-related Polinton and Gypsy elements. It finds 10 fossils in the human genome (8 from TEs and 2 from host genes) that predate the last common ancestor of all jawed vertebrates, probably from the Ordovician period. It also finds types of transposon and retrotransposon not found in human before. These fossils have extreme sequence conservation, indicating exaptation: some have evidence of gene-regulatory function, and they tend to lienearest to developmental genes. Some ancient fossils suggest “genome tectonics”, where two fragments of one TE have drifted apart by up to megabases, possibly explaining gene deserts and large introns. This paints a picture of great TE diversity in our aquatic ancestors, with patchy TE inheritance by later vertebrates, producing new genes and regulatory elements on the way. Host-gene fossils too have contributed anciently-conserved DNA segments. This paves the way to further studies of ancient protein fossils.

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Paleovirology of the DNA viruses of eukaryotes

Cited by 22 publications

References 102 publications

Pif1 Helicases and the Evidence for a Prokaryotic Origin of Helitrons

Pif1 Helicases and the Evidence for a Prokaryotic Origin of Helitrons

Virophages and retrotransposons colonize the genomes of a heterotrophic flagellate

Paleozoic Protein Fossils Illuminate the Evolution of Vertebrate Genomes and Transposable Elements

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