Damage and degradation rates of extracellular DNA in marine sediments: implications for the preservation of gene sequences

Abstract

The extracellular DNA pool in marine sediments is the largest reservoir of DNA of the world oceans and it potentially represents an archive of genetic information and gene sequences involved in natural transformation processes. However, no information is at present available for the gene sequences contained in the extracellular DNA and for the factors that influence their preservation. In the present study, we investigated the depurination and degradation rates of extracellular DNA in a variety of marine sediment samples characterized by different ages (up to 10 000 years) and environmental conditions according to the presence, abundance and diversity of prokaryotic gene sequences. We provide evidence that depurination of extracellular DNA in these sediments depends upon the different environmental factors that act synergistically and proceeds at much slower rates than those theoretically predicted or estimated for terrestrial ecosystems. These findings suggest that depurination in marine sediments is not the main process that limits extracellular DNA survival. Conversely, DNase activities were high suggesting a more relevant role of biologically driven processes. Amplifiable prokaryotic 16S rDNA sequences were present in most benthic systems analysed, independent of depurination and degradation rates and of the ages of the sediment samples. Additional molecular analyses revealed that the extracellular DNA pool is characterized by relatively low‐copy numbers of prokaryotic 16S rDNA sequences that are highly diversified. Overall, our results suggest that the extracellular DNA pool in marine sediments represents a repository of genetic information, which can be used for improving our understanding of the biodiversity, functioning and evolution of ecosystems over different timescales.