Microbial community assembly in marine sediments

Abstract

Marine sediments are densely populated by diverse communities of archaea and bacteria, with intact cells detected kilometers below the seafloor. Analyses of microbial diversity in these unique environments have identified several dominant taxa that comprise a significant portion of the community in geographically and environmentally disparate locations. While the distributions of these populations are well documented, there is significantly less information describing the means by which such specialized communities assemble within the sediment column. Here, we review known patterns of subsurface microbial community composition and perform a meta-analysis of publicly available 16S rRNA gene datasets collected from 9 locations at depths from 1 cm to > 2 km below the surface. All data are discussed in relation to the 4 major processes of microbial community assembly: diversification, dispersal, selection, and drift. Microbial diversity in the subsurface decreases with depth on a global scale. The transition from the seafloor to the deep subsurface biosphere is marked by a filtering of populations from the surface that leaves only a subset of taxa to populate the deeper sediment zones, indicating that selection is a main mechanism of community assembly. The physiological underpinnings for the success of these persisting taxa are largely unknown, as the majority of them lack cultured representatives. Ecological explanations for the observed trends are presented, including the possible influence of energy depletion and the physiological basis of major taxonomic shifts.

Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time

“…It is the continual worsening of conditions over time and burial that has led to dormancy in the marine subsurface being likened to a "dead-end strategy" (Jørgensen, 2012). The estimated generation times for the deep biosphere, up to several thousands of years (Braun et al, 2017;Trembath-Reichert et al, 2017;Biddle et al, 2006;Jorgensen, D'Hondt, & Miller, 2006;Jørgensen, 2011;Lomstein et al, 2012;Whitman, Coleman, & Wiebe, 1998;Xie, Lipp, Wegener, Ferdelman, & Hinrichs, 2013), necessitate very low mutation rates, and therefore, selection is likely dominated by the presence of pre-adapted sub-seafloor taxa (Orsi, 2018;Petro, Starnawski, Schramm, & Kjeldsen, 2017). Further, whether these generation times reflect actual growth (i.e., new biomass generation from cellular division) or replacement (i.e., turnover of biomolecules without division, akin to maintenance activities) is not known.…”

Glacial runoff promotes deep burial of sulfur cycling-associated microorganisms in marine sediments

“…Microbial communities in the NGI sediments became less diverse with depth and increasingly distinct from the surface communities (Supplementary Figure S2). Such shifts in community composition with depth can be attributed to the progressing geochemical stratification of the sediment and decreasing flux of energy with increasing sediment age (Petro et al, 2017).…”

“…In sediments with comparably slow sediment accumulation, which typify non-glaciated Arctic shelf areas (Kuzyk et al, 2013), the rate of organic matter mineralization is highest at the surface and decreases significantly with increasing sediment depth (Kuzyk et al, 2017; Lomstein et al, 2012), reflecting a concomitant decrease in energy available for cell maintenance and growth (Starnawski et al, 2017). This depth gradient results in pronounced compositional changes in the benthic microbial community, which are driven by highly selective survival of microorganisms that are able to subsist in the energy-limited subsurface (Bird et al, 2019; Marshall et al, 2019; Petro et al, 2017; Starnawski et al, 2017). Here, we hypothesized that this strong environmental filtering effect would be attenuated in sediments with high rates of sedimentation (i.e., in coastal sediments impacted by glacial runoff) and result in a different pattern of microbial community assembly with depth.…”

Marine deep biosphere microbial communities assemble in near-surface sediments in Aarhus Bay

“…The OTUs which increased in absolute abundance with depth ( Supplementary Table 1) 380 belong to common subsurface lineages such as the Atribacteria and members of the 381 class Phycisphaerae, both of which have been found to constitute a significant portion 382 of the microbial community hundreds of meters below the seafloor (Petro et al, 2017). 383 384…”