Overballe-Petersen, Søren5; Harms, Klaus6; Orlando, Ludovic Antoine Alexandre5; Mayar, J. Victor Moreno5; Rasmussen, Simon1; Dahl, Tais Wittchen5; Rosing, Minik Thorleif5; Poole, Anthony M7; Sicheritz-Pontén, Thomas1; Brunak, Søren1; Inselmann, Sabrina8; de Vries, Johann8; Wackernagel, Wilfried8; Pybus, Oliver G9; Nielsen, Rasmus10; Johnsen, Pål Jarle6; Nielsen, Kaare Magne6; Willerslev, Eske5
1 Department of Systems Biology, Technical University of Denmark2 Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark3 Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark4 CFB - Metagenomic Systems Biology, Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark5 University of Copenhagen6 University of Tromsø7 University of Canterbury8 Carl von Ossietzky Universität Oldenburg9 University of Oxford10 University of California
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, doublenucleotide 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.
Proceedings of the National Academy of Sciences of the United States of America, 2013, Vol 110, Issue 49, p. 19860-19865