AbstractDNA in marine sediment contains both fossil sequences and sequences from organisms that live in the sediment. The demarcation between these two pools and their respective rates of turnover are generally unknown. We address these issues by comparing the total extractable DNA pool to the fraction of sequenced chloroplast DNA (cpDNA) in sediment from two sites in the Bering Sea. We assume that cpDNA is a tracer of non-reproducing fossil DNA. Given >150,000 sequence reads per sample, cpDNA is easily detectable in the shallowest samples but decays with depth, suggesting that sequencing-based richness assessments of communities in deep subseafloor sediment are relatively unaffected by fossil DNA. The initial decrease in cpDNA reads suggests that most cpDNA decays within 100–200 k.y. of deposition. However, cpDNA from a few phylotypes, including some that match fossil diatoms, are present throughout the cored sediment, ranging in age to 1.4 Ma. The relative fraction of sequences composed by cpDNA decreases non-linearly with increasing sediment age, suggesting that detectable cpDNA becomes more recalcitrant with age. This can be explained by biological activity decreasing with sediment age and/or by preferential long-term survival of only the most thoroughly protected DNA. The association of cpDNA reads with published records of siliceous microfossils, including diatom spores, at the same sites suggests that microfossils may help to preserve DNA. This DNA may be useful for studies of paleoenvironmental conditions and biological evolution on time scales that approach or exceed 1 m.y.
Subseafloor sediment hosts a large, taxonomically rich and metabolically diverse microbial ecosystem. However, the factors that control microbial diversity in subseafloor sediment have rarely been explored. Here we show that bacterial richness varies with organic degradation rate and sediment age. At three open-ocean sites (in the Bering Sea and equatorial Pacific) and one continental margin site (Indian Ocean), richness decreases exponentially with increasing sediment depth. The rate of decrease in richness with depth varies from site to site. The vertical succession of predominant terminal electron acceptors correlates to abundance-weighted community composition, but does not drive the vertical decrease in richness. Vertical patterns of richness at the open-ocean sites closely match organic degradation rates; both properties are highest near the seafloor and decline together as sediment depth increases. This relationship suggests that (i) total catabolic activity and/or electron donor diversity exerts a primary influence on bacterial richness in marine sediment, and (ii) many bacterial taxa that are poorly adapted for subseafloor sedimentary conditions are degraded in the geologically young sediment where respiration rates are high. Richness consistently takes a few hundred thousand years to decline from near-seafloor values to much lower values in deep anoxic subseafloor sediment, regardless of sedimentation rate, predominant terminal electron acceptor, or oceanographic context.
Importance Subseafloor sediment provides a wonderful opportunity to investigate drivers of microbial diversity in communities that may be isolated for millions of years. Our manuscript shows the impact of in situ conditions on bacterial community structure in subseafloor sediment. Specifically, it shows that bacterial richness in subseafloor sediment declines exponentially with sediment age, and in parallel with organic-fueled oxidation rate. This result suggests that subseafloor diversity ultimately depends on electron donor diversity and/or total community respiration. Despite the extraordinary nature of this ecosystem, we believe this is the first study of how and why biological richness changes over time in subseafloor sediment.