Bacterial natural transformation by highly fragmented and damaged DNA

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

doi:10.1073/pnas.1315278110

Bacterial natural transformation by highly fragmented and damaged DNA

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

Computational and RNA Biology

92 Citations (Scopus)

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, 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.

Original language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	110
Issue number	49
Pages (from-to)	19860–19865
Number of pages	6
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1315278110
Publication status	Published - 3 Dec 2013

Access to Document

10.1073/pnas.1315278110

19860.full.pdfFinal published version, 945 KB

Cite this

Overballe-Petersen, S., Harms, K., Orlando, L. A. A., Moreno Mayar, J. V., Rasmussen, S., Dahl, T. W., Rosing, M. T., Poole, A. M., Sicheritz-Ponten, T., Brunak, S., Inselmann, S., de Vries, J., Wackernagel, W., Pybus, O. G., Nielsen, R., Johnsen, P. J., Nielsen, K. M., & Willerslev, E. (2013). Bacterial natural transformation by highly fragmented and damaged DNA. Proceedings of the National Academy of Sciences of the United States of America, 110(49), 19860–19865 . https://doi.org/10.1073/pnas.1315278110

Bacterial natural transformation by highly fragmented and damaged DNA. / Overballe-Petersen, Søren; Harms, Klaus; Orlando, Ludovic Antoine Alexandre et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 110, No. 49, 03.12.2013, p. 19860–19865 .

Research output: Contribution to journal › Journal article › Research › peer-review

Overballe-Petersen, S, Harms, K, Orlando, LAA, Moreno Mayar, JV , Rasmussen, S , Dahl, TW , Rosing, MT, Poole, AM, Sicheritz-Ponten, T, Brunak, S, Inselmann, S, de Vries, J, Wackernagel, W, Pybus, OG, Nielsen, R, Johnsen, PJ, Nielsen, KM & Willerslev, E 2013, 'Bacterial natural transformation by highly fragmented and damaged DNA', Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 49, pp. 19860–19865 . https://doi.org/10.1073/pnas.1315278110

@article{e597929628554af7a5e6602d4068486c,

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, 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.",

author = "S{\o}ren Overballe-Petersen and Klaus Harms and Orlando, {Ludovic Antoine Alexandre} and {Moreno Mayar}, {Jos{\'e} Victor} and Simon Rasmussen and Dahl, {Tais W.} and Rosing, {Minik Thorleif} and Poole, {Anthony M.} and Thomas Sicheritz-Ponten and S{\o}ren Brunak and Sabrina Inselmann and {de Vries}, Johann and Wilfried Wackernagel and Pybus, {Oliver G.} and Rasmus Nielsen and Johnsen, {P{\aa}l Jarle} and Nielsen, {Kaare Magne} and Eske Willerslev",

year = "2013",

month = dec,

day = "3",

doi = "10.1073/pnas.1315278110",

language = "English",

volume = "110",

pages = "19860–19865 ",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "The National Academy of Sciences of the United States of America",

number = "49",

}

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 -

Bacterial natural transformation by highly fragmented and damaged DNA

Abstract

Access to Document

Fingerprint

Cite this