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.

Keywords: diagenesis; manganese (oxyhydr)oxides; microbial communities; trace metals.

FIGURE 1

Location of multi‐corer cores PS119_14‐1 and PS119_15‐2 collected from the East Scotia Ridge (ESR) during R/V Polarstern Expedition PS119. The yellow star indicates the location of Site PS119_15‐2, and the red, solid box indicates the location of Site PS119_14_1. The nine segments of the East Scotia Ridge hydrothermal vent system are labeled E1–E9 and marked by gray lines based on segment positions in German et al. (2000). Study area relative to South America, Africa, and Antarctica is denoted by the red box and red star in the inset map found at the lower left. Bottom panel depicts the sampling locations of both cores and the topography, based on echosounder data, along a 14.4 nautical mile, NW‐SE cross section. Black, leftward arrow indicates the direction towards the E2 Segment of the ESR, and the black, rightward arrow indicates the direction towards the South Sandwich Island Arc.

FIGURE 2

Schematic of the sampling, incubation, and analytical procedures. Samples were recovered with a multi‐corer. Recovered cores were ~35 cm in length spanning from the sediment–water interface at 0 cm below seafloor (cmbsf) to 35 cmbsf. Cores were then sectioned using sterile tools into 50 mL centrifuge tubes, sealed in nitrogen flushed aluminum foil bags, and stored at 4°C for an incubation period (directly after sampling, t ₀, 4 months, t ₁, and 8 months, t ₂). Following incubation, porewater was extracted using Rhizons for analysis of sulfate (SO₄ ²⁻) alkalinity (only t ₀ samples*), and metal concentrations. After porewater extraction, a sediment split was removed for inorganic geochemical analysis of total organic carbon (TOC) and metal content, and the remaining sediment was preserved for 16S rRNA analysis.

FIGURE 3

Solid phase metal content ranges at Sites PS119_14‐1 (gray) and PS119_15‐2 (red). The colored rectangles show 25%–27% of the occurrence with the horizontal line as the median line, the range within 1.5 interquartile range shown by the vertical line, rhombus indicates outliers, small squares depict the median value.

FIGURE 4

Total organic carbon (TOC) content and porewater sulfate (SO₄ ²⁻) concentrations at Sites (A) PS119_14‐1 and (B) PS119_15‐2. All depths are in centimeters below seafloor (cmbsf). Samples were measured at 0 months (t ₀) (blue circles), 4 months (t ₁) (orange squares), and 8 months (t ₂) (gray diamonds) incubation.

FIGURE 5

Porewater concentration profiles of manganese (Mn), vanadium (V), chromium (Cr), cobalt (Co), nickel (Ni), copper (Cu), arsenic (As), molybdenum (Mo), silver (Ag), cadmium (Cd), thallium (Tl), and uranium (U) at Site PS119_14‐1. All depths are in centimeters below seafloor (cmbsf). Samples were measured at 0 months (t ₀) (blue circle), 4 months (t ₁) (orange square), and 8 months (t ₂) (gray diamond) incubation.

FIGURE 6

Porewater concentration profiles of manganese (Mn) (note the break in the Y‐scale), vanadium (V), chromium (Cr), cobalt (Co), nickel (Ni), copper (Cu), arsenic (As), molybdenum (Mo), silver (Ag), cadmium (Cd), thallium (Tl) (note the break in the Y‐scale), and uranium (U) at Site PS119_15‐2. All depths are in centimeters below seafloor (cmbsf). Samples were measured at 0 months (t ₀) (blue circle), 4 months (t ₁) (orange square), and 8 months (t ₂) (gray diamond) incubation.

FIGURE 7

Taxonomic distribution at the class level of all the ASVs identified in the samples from PS119_14‐1. The left six columns labeled t ₀“sample” (e.g., t ₀ 2–5 cm) represent the 6 depths sampled for 16S rRNA gene sequencing from the initial, non‐incubated core. The right five columns, labeled t ₂“sample” (e.g., t ₂ 0–1 cm) represent the 5 corresponding depths incubated for 8 months and sampled for 16S rRNA gene sequencing.

FIGURE 8

Non‐metric multidimensional scaling (NMDS) of t ₀ (red) and t ₂ (blue) samples from PS119_14‐1. Each measured metal is plotted as a vector, where the length and direction indicate the contribution of the variable to the principal component. Significant variables, as p‐values, are labeled as: *** = 0 < value ≤ 0.001, ** < 0.001, * < 0.01, and +< 0.05.

FIGURE 9

Correlation between each of the 50 most abundant ASV with the trace metal concentrations (left panel) and relative abundance in the core and incubation samples of each ASV (right panel) from PS119_14‐1 t ₀ (red circles; Core) and t ₂ (blue circles; Incubation) samples. Metals were clustered based on their concentrations. Only correlations with a p‐value < 0.05 are displayed.