Bacterial natural transformation by highly fragmented and damaged DNA

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 110; no. 49; pp. 19860 - 19865
• Main Authors: Overballe-Petersen, Søren, Harms, Klaus, Orlando, Ludovic A. A., Mayar, J. Victor Moreno, Rasmussen, Simon, Dahl, Tais W., Rosing, Minik T., Poole, Anthony M., Sicheritz-Ponten, Thomas, Brunak, Søren, Inselmann, Sabrina, de Vries, Johann, Wackernagel, Wilfried, Pybus, Oliver G., Nielsen, Rasmus, Johnsen, Pål Jarle, Nielsen, Kaare Magne, Willerslev, Eske
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 03.12.2013; NATIONAL ACADEMY OF SCIENCES; National Acad Sciences
• Subjects: Acinetobacter; Acinetobacter - genetics; Animals; Bacteria; Base Sequence; Biological Sciences; Deoxyribonucleic acid; DNA; DNA - genetics; DNA - metabolism; DNA damage; DNA Damage - genetics; DNA Primers - genetics; Evolution; Evolution, Molecular; Gene Transfer, Horizontal - genetics; Genetic mutation; Genomes; Gram-negative bacteria; Mammoths - genetics; Molecular Sequence Data; Molecules; Nucleotides; Polymorphism; Sequence Analysis, DNA; Sequencing; Transformation, Bacterial - genetics; microbial evolution; DNA degradation; anachronistic evolution; horizontal gene transfer; early life
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1315278110

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.