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Bacterial natural transformation by highly fragmented and damaged DNA
Edited* by P. Buford Price, University of California, Berkeley, CA, and approved October 15, 2013 (received for review August 14, 2013)
Significance
Short and damaged DNA is ubiquitous in most environments and can survive more than half a million years. We show that naturally competent environmental bacteria can take up such degraded DNA and incorporate it into their genomes, including DNA from a 43,000-y-old woolly mammoth bone. The process occurs as part of cellular DNA replication and may resemble the earliest forms of horizontal gene transfer. Our findings suggest that natural genetic exchange of DNA from dead and even extinct organisms to contemporary bacteria can take place over hundreds of thousands of years. Hence damaged and degraded DNA may be a previous unrecognized driver of bacterial evolution with implications for evolutionary theory.
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, 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.
Footnotes
↵1S.O.-P. and K.H. contributed equally to this work.
↵2Present address: Klinik für Hämatologie, Onkologie und Immunologie, Philipps Universität Marburg and Universitätsklinkum Gießen und Marburg Standort Marburg, 35033 Marburg, Germany.
- ↵3To whom correspondence may be addressed. E-mail: ewillerslev{at}snm.ku.dk or kaare.nielsen{at}uit.no.
Author contributions: E.W. conceived and headed the project; S.O.-P., K.H., L.A.A.O., P.J.J., K.M.N., and E.W. designed research; S.O.-P. and K.H. did the experimental work; S.R., T.S.-P., and S.B. did the genome mapping and assembly; J.V.M.M. did the genome analysis and statistics; S.I., J.d.V., and W.W. contributed to the results presented in Fig. 1 and Fig. S1; S.O.-P. produced the figures; S.O.-P., K.H., J.V.M.M., S.R., A.M.P., T.S.-P., S.B., O.G.P., and R.N. analyzed data; and S.O.-P., K.H., T.W.D., M.T.R., O.G.P., P.J.J., K.M.N., and E.W. wrote the paper.
The authors declare no conflict of interest.
↵*This Direct Submission article had a prearranged editor.
Data deposition: The sequence data have been deposited with the European Nucleotide Archive, www.ebi.ac.uk/ena (accession no. PRJEB4698).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1315278110/-/DCSupplemental.
Freely available online through the PNAS open access option.