Bacterial natural transformation by highly fragmented and damaged DNA

TY - JOUR

T1 - Bacterial natural transformation by highly fragmented and damaged DNA

AU - Overballe-Petersen, Søren

AU - Harms, Klaus

AU - Orlando, Ludovic Antoine Alexandre

AU - Moreno Mayar, José Victor

AU - Rasmussen, Simon

AU - Dahl, Tais W.

AU - Rosing, Minik Thorleif

AU - Poole, Anthony M.

AU - Sicheritz-Ponten, Thomas

AU - Brunak, Søren

AU - Inselmann, Sabrina

AU - de Vries, Johann

AU - Wackernagel, Wilfried

AU - Pybus, Oliver G.

AU - Nielsen, Rasmus

AU - Johnsen, Pål Jarle

AU - Nielsen, Kaare Magne

AU - Willerslev, Eske

PY - 2013/12/3

Y1 - 2013/12/3

N2 - 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.

AB - 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.

U2 - 10.1073/pnas.1315278110

DO - 10.1073/pnas.1315278110

M3 - Journal article

C2 - 24248361

SN - 0027-8424

VL - 110

SP - 19860

EP - 19865

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 49

ER -