Relationship of Bacterial Richness to Organic Degradation Rate and Sediment Age in Subseafloor Sediment

Abstract

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 increasing depth varies from site to site. The vertical succession of predominant terminal electron acceptors correlates with 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 the drivers of microbial diversity in communities that may have been isolated for millions of years. Our paper 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. This work studied how and why biological richness changes over time in the extraordinary ecosystem of subseafloor sediment.

Abrupt burial imparts persistent changes to the bacterial diversity of turbidite‐associated sediment profiles

“…The persistence of cell displacement signatures with turbidite deposition suggests historical changes in seed populations may be detected indefinitely in modern community profiles. Together with previous studies observing sediment preservation of changes to water‐column communities (Hamdan et al., ; Walsh et al., ; Orsi et al., ), this study encourages further investigation of modern microbial communities in sediments deposited at times of substantial environmental change. Both the dormant and active microbial populations may preserve genetic information concerning paleoenvironmental conditions.…”

“…In contrast, DNA signatures from historical events that modify the abundance or dispersal of cells viable in deep surface environments may be preserved indefinitely through the inheritance of genetic information in successive populations, limited only by competition in situ and emigration of cells with fluid advection. Recent studies have linked broad changes in water‐column conditions to subsurface diversity in lacustrine (Thomas, Ionescu, & Ariztegui, ) and marine environments (Hamdan et al., ; Walsh et al., ). Orsi et al.…”

Microbial community assembly in marine sediments

“…A similar relationship between microbial diversity and organic matter availability has been demonstrated in previous research, such as a study of Arctic deep-sea sediments which identified a positive response of bacterial OTU richness to increased phytodetrital input (Bienhold et al 2012). A more recent analysis from 4 sites of the Integrated Ocean Drilling Program could directly correlate the depth-driven exponential decline in microbial richness with organic matter degradation rates, providing direct evidence that organic matter availability may drive the vertical drop in richness (Walsh et al 2016b). The productivity of the overlying water column has also been linked to sedimentary community composition, suggesting that different microbial taxa have varying fitness responses to energy limitations (Polymenakou et al 2005, Bienhold et al 2012.…”

“…This study, which extended to a depth of 6 m below the seafloor (mbsf), found taxonomic richness estimates to be highest in the overlying water column and lowest in the deepest sediment samples taken. A more recent analysis found a similar pattern of decreasing richness with depth, with deeper extension into the sediment column (Walsh et al 2016b). Here, we see the same trends on a global scale.…”

“…Such studies have identified a vertical succession of subsurface populations, re sulting in communities from a given depth having similar composition regardless of geographic location or geochemical conditions. A recent analysis of this vertical succession found that sediment age and organic degradation rates exert primary control on changes in bacterial richness, with all properties declining with sediment depth (Walsh et al 2016b). …”