Holocene paleodepositional changes reflected in the sedimentary microbiome of the Black Sea

Subsurface microbial communities are generally thought to be structured through in situ environmental conditions such as the availability of electron acceptors and donors and porosity, but recent studies suggest that the vertical distribution of a subset of subseafloor microbial taxa, which were present at the time of deposition, were selected by the paleodepositional environment. However, additional highly resolved temporal records of subsurface microbiomes and paired paleoenvironmental reconstructions are needed to justify this claim. Here, we performed a highly resolved shotgun metagenomics survey to study the taxonomic and functional diversity of the subsurface microbiome in Holocene sediments underlying the permanently stratified and anoxic Black Sea. Obligate aerobic bacteria made the largest contribution to the observed shifts in microbial communities associated with known Holocene climate stages and transitions. This suggests that the aerobic fraction of the subseafloor microbiome was seeded from the water column and did not undergo post-depositional selection. In contrast, obligate and facultative anaerobic bacteria showed the most significant response to the establishment of modern-day environmental conditions 5.2 ka ago that led to a major shift in planktonic communities and in the type of sequestered organic matter available for microbial degradation. No significant shift in the subseafloor microbiome was observed as a result of environmental changes that occurred shortly after the marine reconnection, 9 ka ago. This supports the general view that the marine reconnection was a gradual process. We conclude that a high-resolution analysis of downcore changes in the subseafloor microbiome can provide detailed insights into paleoenvironmental conditions and biogeochemical processes that occurred at the time of deposition.