Published November 6, 2013 | Version v1
Journal article Restricted

Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

  • 1. Laboratoire ‘Microorganismes: Ge´nome et Environnement’, Clermont Universite´, Universite´ Blaise Pascal, Clermont-Ferrand 63000, France and CNRS UMR 6023, LMGE, Aubie`re 63171, France
  • 2. UPMC (Paris-06) and CNRS, UMR 7144, Station Biologique, Roscoff 29680, France
  • 3. Unite´ Biologie Mole´culaire du Ge`ne chez les Extreˆmophiles, De´partement de Microbiologie, Institut Pasteur, 25 rue du Dr. Roux, Paris 75015, France and Laboratoire de Biologie Mole´culaire du Ge`ne chez les Extreˆmophiles, Institut de Ge´ne´tique et Microbiologie, CNRS UMR 8621, Universite´ Paris Sud, Orsay 91405, France
  • 4. Unite´ Biologie Mole´culaire du Ge`ne chez les Extreˆmophiles, De´partement de Microbiologie, Institut Pasteur, 25 rue du Dr. Roux, Paris 75015, France

Description

Metagenomic studies have uncovered an astonishing diversity of ssDNA viruses encoding
replication proteins (Reps) related to those of eukaryotic Circoviridae, Geminiviridae or
Nanoviridae; however, exact evolutionary relationships among these viruses remain obscure.
Recently, a unique chimeric virus (CHIV) genome, which has apparently emerged via
recombination between ssRNA and ssDNA viruses, has been discovered. Here we report on
the assembly of 13 new CHIV genomes recovered from various environments. Our results
indicate a single event of capsid protein (CP) gene capture from an RNA virus in the history of
this virus group. The domestication of the CP gene was followed by an unprecedented
recurrent replacement of the Rep genes in CHIVs with distant counterparts from diverse
ssDNA viruses. We suggest that parasitic and symbiotic interactions between unicellular
eukaryotes were central for the emergence of CHIVs and that such turbulent evolution was
primarily dictated by incongruence between the CP and Rep proteins.

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Funding

MICRO B3 – Marine Microbial Biodiversity, Bioinformatics and Biotechnology 287589
European Commission