Bacterial natural transformation by highly fragmented and damaged DNA

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Søren Overballe-Petersen, Klaus Harms, Ludovic Antoine Alexandre Orlando, José Victor Moreno Mayar, Simon Rasmussen, Tais W. Dahl, Minik Thorleif Rosing, Anthony M. Poole, Thomas Sicheritz-Ponten, Søren Brunak, Sabrina Inselmann, Johann de Vries, Wilfried Wackernagel, Oliver G. Pybus, Rasmus Nielsen, Pål Jarle Johnsen, Kaare Magne Nielsen, Eske Willerslev

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.
OriginalsprogEngelsk
TidsskriftProceedings of the National Academy of Sciences of the United States of America
Vol/bind110
Udgave nummer49
Sider (fra-til)19860–19865
Antal sider6
ISSN0027-8424
DOI
StatusUdgivet - 3 dec. 2013

ID: 81395546