Impacts on Sedimentary Microbial Communities Related to Temporal Changes in Trace Metal Concentrations

Abstract

Microbial processes in marine sediments drive changes in redox conditions, ultimately controlling the cycling of elements between the dissolved and solid phases. The microbial community driving these cycles depends on trace metals, but it can also be inhibited at elevated metal concentrations. During diagenesis, many trace elements are released from iron (Fe) and manganese (Mn) (oxyhydr)oxides, potentially affecting microbial metabolisms. Here we present results from geochemical and microbiological analyses of samples collected during R/V Polarstern Expedition PS119 to the East Scotia Ridge. The sediments are dominantly diatomaceous ooze with high contents of reactive Fe and Mn (oxyhydr)oxides and increased trace metal contents from nearby hydrothermal vents. Two multi-corer cores were sampled immediately after collection at five specific sediment depths (three splits each), sealed anaerobically in incubation bags, and analyzed in 4-month intervals post collection for major, minor, and trace metals and 16S rRNA gene sequencing. By isolating the sediment from overlying seawater during the incubation process, we simulated the in situ diagenetic processes of Fe and Mn oxide reduction. Our data show that Mn and trace metals, especially Mo, Ni, Tl, and Cu, are mobilized during early diagenesis. Analysis of 16S rRNA genes revealed shifts in the microbial community from Nitrososphaera and Nanoarchaeia to Bacteroidia and Bacilli alongside a marked decrease in richness, Pielou's evenness, and Shannon alpha diversity during the eight-month incubations. We statistically correlate the microbial community shift with the changes in porewater trace metal concentrations, revealing that Mn, Co, Ag, and Tl are driving the microbial compositions in these samples. In this organic matter limited but Fe and Mn (oxyhydr)oxide rich system, we simulate deeper diagenesis to peer into the role of changing Fe, Mn, and trace metal cycles and highlight the role of Fe and Mn (oxyhdyr)oxides as shuttles for trace metals to the deep biosphere. By identifying key metals that are diagenetically cycled and affect the in situ microbial community, we reveal feedbacks between metals and microbial communities that play important roles in biogeochemical cycles on Earth, provide insight into the origin and potential evolution of metabolic pathways in the deep biosphere, and offer clues that may aid in our understanding of Earth's history and potentially beyond.