title: Bacterial natural transformation by highly fragmented and damaged DNA.
abstract: DNA molecules are continuously released through decomposition of organic matter and are ubiquitous in most environments. Such DNA becomes fragmented and damaged (often <100 bp) and may persist in the environment for more than half a million years. Fragmented DNA is recognized as nutrient source for microbes, but not as potential substrate for bacterial evolution. Here, we show that fragmented DNA molecules (≥ 20 bp) that additionally may contain abasic sites, cross-links, or miscoding lesions are acquired by the environmental bacterium Acinetobacter baylyi through natural transformation. With uptake of DNA from a 43,000-y-old woolly mammoth bone, we further demonstrate that such natural transformation events include ancient DNA molecules. We find that the DNA recombination is RecA recombinase independent and is directly linked to DNA replication. We show that the adjacent nucleotide variations generated by uptake of short DNA fragments escape mismatch repair. Moreover, double-nucleotide polymorphisms appear more common among genomes of transformable than nontransformable bacteria. Our findings reveal that short and damaged, including truly ancient, DNA molecules, which are present in large quantities in the environment, can be acquired by bacteria through natural transformation. Our findings open for the possibility that natural genetic exchange can occur with DNA up to several hundreds of thousands years old.
authors.affiliation: Centre for GeoGenetics and Nordic Center for Earth Evolution, University of Copenhagen, 1350 Copenhagen K, Denmark.
authors.forename: Søren
authors.initials: S
authors.lastname: Overballe-Petersen
authors.forename: Klaus
authors.initials: K
authors.lastname: Harms
authors.forename: Ludovic A A
authors.initials: LA
authors.lastname: Orlando
authors.forename: J Victor Moreno
authors.initials: JV
authors.lastname: Mayar
authors.forename: Simon
authors.initials: S
authors.lastname: Rasmussen
authors.forename: Tais W
authors.initials: TW
authors.lastname: Dahl
authors.forename: Minik T
authors.initials: MT
authors.lastname: Rosing
authors.forename: Anthony M
authors.initials: AM
authors.lastname: Poole
authors.forename: Thomas
authors.initials: T
authors.lastname: Sicheritz-Ponten
authors.forename: Søren
authors.initials: S
authors.lastname: Brunak
authors.forename: Sabrina
authors.initials: S
authors.lastname: Inselmann
authors.forename: Johann
authors.initials: J
authors.lastname: de Vries
authors.forename: Wilfried
authors.initials: W
authors.lastname: Wackernagel
authors.forename: Oliver G
authors.initials: OG
authors.lastname: Pybus
authors.forename: Rasmus
authors.initials: R
authors.lastname: Nielsen
authors.forename: Pål Jarle
authors.initials: PJ
authors.lastname: Johnsen
authors.forename: Kaare Magne
authors.initials: KM
authors.lastname: Nielsen
authors.forename: Eske
authors.initials: E
authors.lastname: Willerslev
mesh_terms: D000150:Acinetobacter / Q000235:genetics*; D000818:Animals; D001483:Base Sequence; D004247:DNA / Q000235:genetics / Q000378:metabolism*; D004249:DNA Damage / Q000235:genetics*; D017931:DNA Primers / Q000235:genetics; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal / Q000235:genetics*; D056665:Mammoths / Q000235:genetics; D008969:Molecular Sequence Data; D017422:Sequence Analysis, DNA; D014169:Transformation, Bacterial / Q000235:genetics*
chemical_list: D017931:DNA Primers; D004247:DNA
keywords: DNA degradation; anachronistic evolution; early life; horizontal gene transfer; microbial evolution