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. microbial evolution | horizontal gene transfer | DNA degradation | early life | anachronistic evolution

Scientific Opinion on application (EFSA‐GMO‐BE‐2011‐101) for the placing on the market of herbicide‐tolerant genetically modified oilseed rape MON 88302 for food and feed uses, import and processing under Regulation (EC) No 1829/2003 from Monsanto

“…A single alignment with A. tumefaciens Ti-plasmid sequence of sufficient length and identity for HR (de Vries and Wackernagel, 2002;Monier et al, 2007;Hülter and Wackernagel, 2008;EFSA, 2009b;Overballe-Petersen et al, 2013) was identified, as expected. The alignment displayed 99.3 % identity over a 296 bp fragment of the Ti-plasmid containing the left border region used for transfer of the T-DNA.…”

Growth phase-specific evolutionary benefits of natural transformation in Acinetobacter baylyi

“…All the fitness values on group and single population levels are listed in Supplementary Table SI 5, respectively. In a control experiment ADP1200Com+ generated on average 2655 transformants per milliliter yielding a frequency of 2.7 × 10 -5 transformants per recipient (that is, natural transformation occurred below saturated DNA concentrations (Overballe-Petersen, Harms et al, 2013).…”

Silencing of natural transformation by an RNA chaperone and a multitarget small RNA

“…Active acquisition of random parts of the genetic material released by phylogenetically close organisms produces genetic polymorphism and functions as "localized sex" in reference to the function of sex in eukaryotic organisms (2). In addition, evidence suggests that genetic transformation can also occur with distantly related and even damaged DNA (3,4). Depending on the bacteria's biotope, the constant and random acquisition of genetic material could be as harmful as it is beneficial, and in most transformable species, natural transformation is a strictly regulated process (1,5).…”