Preservation and Significance of Extracellular DNA in Ferruginous Sediments from Lake Towuti, Indonesia

Abstract

Extracellular DNA is ubiquitous in soil and sediment and constitutes a dominant fraction of environmental DNA in aquatic systems. In theory, extracellular DNA is composed of genomic elements persisting at different degrees of preservation produced by processes occurring on land, in the water column and sediment. Extracellular DNA can be taken up as a nutrient source, excreted or degraded by microorganisms, or adsorbed onto mineral matrices, thus potentially preserving information from past environments. To test whether extracellular DNA records lacustrine conditions, we sequentially extracted extracellular and intracellular DNA from anoxic sediments of ferruginous Lake Towuti, Indonesia. We applied 16S rRNA gene Illumina sequencing on both fractions to discriminate exogenous from endogenous sources of extracellular DNA in the sediment. Environmental sequences exclusively found as extracellular DNA in the sediment originated from multiple sources. For instance, Actinobacteria, Verrucomicrobia, and Acidobacteria derived from soils in the catchment. Limited primary productivity in the water column resulted in few sequences of Cyanobacteria in the oxic photic zone, whereas stratification of the water body mainly led to secondary production by aerobic and anaerobic heterotrophs. Chloroflexi and Planctomycetes, the main degraders of sinking organic matter and planktonic sequences at the water-sediment interface, were preferentially preserved during the initial phase of burial. To trace endogenous sources of extracellular DNA, we used relative abundances of taxa in the intracellular DNA to define which microbial populations grow, decline or persist at low density with sediment depth. Cell lysis became an important additional source of extracellular DNA, gradually covering previous genetic assemblages as other microbial genera became more abundant with depth. The use of extracellular DNA as nutrient by active microorganisms led to selective removal of sequences with lowest GC contents. We conclude that extracellular DNA preserved in shallow lacustrine sediments reflects the initial environmental context, but is gradually modified and thereby shifts from its stratigraphic context. Discrimination of exogenous and endogenous sources of extracellular DNA allows simultaneously addressing in-lake and post-depositional processes. In deeper sediments, the accumulation of resting stages and sequences from cell lysis would require stringent extraction and specific primers if ancient DNA is targeted.

Transitory microbial habitat in the hyperarid Atacama Desert

“…Two unique methods were used. The e/i-DNA methodology is described in detail in an appropriate subject journal ( 13 ), with some of the associated issues discussed elsewhere ( 40 ). The validity of the e/i-DNA method is further supported by a positive correlation between microbial biomass and the Shannon index (SI) calculated for iDNA ( ), but not with either calcium or sulfate concentrations.…”

Mineral Facilitated Horizontal Gene Transfer: A New Principle for Evolution of Life?

“…In general, silicates have a low point of zero charge, i.e., they are negatively charged in wide pH range, whereas oxides and hydroxides have high point of zero charge, i.e., they are positively charged in a wide pH range ( Figure 2 ). DNA interacts with minerals through its phosphate backbone ( Figures 3A,B ), and the nucleobases ( Figure 3C ) provide only a limited contribution to adsorption ( Vuillemin et al, 2017 ). The phosphate moieties of DNA are positively charged below ∼pH 2 and can interact directly with negatively charged silicates and basal planes of clay minerals at such low pH values.…”

Mineral Facilitated Horizontal Gene Transfer: A New Principle for Evolution of Life?

“…positively charged in wide pH range ( Figure 2). DNA interacts with minerals through its phosphate backbone, and the nucleobases (Figure 3) provide only a limited contribution to adsorption (Vuillemin et al, 2017). The phosphate moieties of DNA are positively charged below ~pH 2 and can interact directly with negatively charged silicates and basal planes of clay minerals.…”