Organisms release DNA both when they live and die. Eventually the DNA disintegrates entirely or it is re-metabolized. There is a constant deposition and decomposition that maintains an environmental pool with large quantities of extracellular DNA, some of which can be thousands of years old. The degrading DNA is fragmented and damaged, often to less than one hundred base pairs. Such DNA is only recognized as microbial nutrients and is not considered as direct contributors to bacterial evolutionary processes. The main study shows natural transformation by very short DNA (≥20bp). Further we also show it by damaged short DNA with abasic sites, crosslinks, and miscoding lesions, which are the most common damages in environmental DNA. This is emphasized by successful natural transformation by 43,000-year-old DNA. We find that the process is a simple variant of natural transformation. On top, we illustrate with fullgenome comparisons that the process has general relevance in extant bacteria. Our findings reveal that the large environmental reservoir of short and damaged DNA retains capacity for natural transformation, even after thousands of years. This describes for the first time a process by which cells can acquire functional genetic signatures of the deeper past. Moreover, not only can old DNA revert microbes to past genotypes, but damaged DNA can also produce new variants of already functional sequences. Besides, DNA fragments carry potential to combine functional domains in new ways. The identified novel pathway of natural transformation represents a basal evolutionary process that only requires growing cells that feed on oligonucleotides; a process that possibly is a primeval type of horizontal gene transfer. In extension, our results also provide mechanistic support to hypotheses of horizontal gene transfer playing an important role early in the evolution of life. The published article explains the chemical structure behind an observed degradation difference between the two purine-nucleotides guanosine and adenosine in ancient DNA. We also point at new uses for high-through-put DNA sequencing in chemistry. In addition to qualitative DNA sequencing, statistical analysis of the numerous sequencing reads yields quantitative measurements of DNA modifying reactions.
Main Research Area:
Natural History Museum of Denmark, Faculty of Science, University of Copenhagen, 2013