Sedimentary DNA can influence evolution:Establishing mineral facilitated horizontal gene transfer as a route to bacterial fitness

Abstract

Horizontal gene transfer is one of the most important drivers of bacterial evolution. Transformation by uptake of extracellular DNA is traditionally not considered to be an effective mode of gene acquisition, simply because extracellular DNA is degraded in a matter of days when it is suspended in e.g. seawater. Mineral surfaces are, however, known to preserve DNA in the environment, and sedimentary ancient DNA studies have solidified that there are considerable amounts of fragmented DNA stored in sediments world-wide. Recently the age span of stored DNA was increased to at least 2 Ma. Here, we highlight that fragmented ancient DNA can be fueling the evolution of contemporary bacteria and advocate to consider this route for genetic variation in evolutionary history. We show that Acinetobacter baylyi can incorporate 60 bp DNA fragments adsorbed to a wide range of common sedimentary minerals and that the transformation frequencies scale with the mineral surface properties. Further, our results point to interfacial geochemical and sedimentologic processes as facilitators of evolutionary innovation where DNA-molecules are specific to the environment and the processes providing new DNA molecules may also provide the need to evolve. In contrast to heritable stochastic mutations as proposed by Darwin, the access by which bacteria acquire new genomic material at times with increased stress and also needs, would indicate a non-random mechanism that may propel evolution in a non-stochastic manner.