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.

Extracellular DNA can preserve the genetic signatures of present and past viral infection events in deep hypersaline anoxic basins

“…Extracellular DNA accumulated in the sediments can contain present and past gene sequences [23,[25][26][27][28]. In the DHAB sediments, the extracellular DNA pool was characterized by a higher diversity of 16S rDNA sequences than the microbial DNA.…”

“…At the same time, a fraction of extracellular DNA can escape the degradation processes and accumulate in the sediments [23,24]. Since high extracellular DNA concentrations have been previously reported in permanently anoxic and hypersaline sediments [16,25], these extreme systems can preserve extracellular DNA [20] and the genetic information contained therein [23,[26][27][28].…”

Bacterial natural transformation by highly fragmented and damaged DNA

“…However, the bacterial recombinational potential with DNA should be seen in the broader context of DNA exposure. Of the vast amounts of free DNA in the environment, the majority will exhibit various stages of degradation (3,35,36). Additionally, threshold levels for biologically significant gene transfer frequencies remains to be established for bacterial systems, and differences in transfer frequencies may have little or no impact on long-term evolutionary outcomes (37).…”

History, applications, methodological issues and perspectives for the use environmental DNA (eDNA) in marine and freshwater environments

“…Nonetheless, the effect of these factors has been studied independently and only one of these studies had measured how covariation of these factors (specific environmental conditions) affects persistence . Other abiotic factors related to the system that can also affect persistence include: stream flow, currents, tidal oscillations, type of sediment, and salinity (Corinaldesi, Beolchini, & Dell'Anno, 2008;Golberg et al, 2011;Barnes et al, 2014). For example, eDNA persistence in freshwater lentic systems has been shown to be as great as 30 days (Ficetola et al, 2008) while for marine systems (open and highly dynamic systems) it only averages approximately seven days (Foote et al, 2012;Thomsen et al, 2012b).…”