Fatimah Sulu-Gambari

Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins

Significance Seasonal hypoxia is increasing in coastal areas worldwide, as more nutrients are delivered to the coastal ocean and water temperatures are rising due to climate change. Hypoxia reaches a particularly harmful stage when sulfide, which is highly toxic for marine life, is released to the bottom water. Here, we document a natural microbial mechanism that counteracts the release of free sulfide, thus preventing the most adverse stage of seasonal hypoxia. Electricity-generating cable bacteria produce a large pool of oxidized sedimentary iron minerals, which efficiently bind free sulfide. As cable bacteria are likely abundant in many seasonally hypoxic basins worldwide, their “firewall” mechanism may be widespread. Seasonal oxygen depletion (hypoxia) in coastal bottom waters can lead to the release and persistence of free sulfide (euxinia), which is highly detrimental to marine life. Although coastal hypoxia is relatively common, reports of euxinia are less frequent, which suggests that certain environmental controls can delay the onset of euxinia. However, these controls and their prevalence are poorly understood. Here we present field observations from a seasonally hypoxic marine basin (Grevelingen, The Netherlands), which suggest that the activity of cable bacteria, a recently discovered group of sulfur-oxidizing microorganisms inducing long-distance electron transport, can delay the onset of euxinia in coastal waters. Our results reveal a remarkable seasonal succession of sulfur cycling pathways, which was observed over multiple years. Cable bacteria dominate the sediment geochemistry in winter, whereas, after the summer hypoxia, Beggiatoaceae mats colonize the sediment. The specific electrogenic metabolism of cable bacteria generates a large buffer of sedimentary iron oxides before the onset of summer hypoxia, which captures free sulfide in the surface sediment, thus likely preventing the development of bottom water euxinia. As cable bacteria are present in many seasonally hypoxic systems, this euxinia-preventing firewall mechanism could be widely active, and may explain why euxinia is relatively infrequently observed in the coastal ocean.

Cable Bacteria Control Iron–Phosphorus Dynamics in Sediments of a Coastal Hypoxic Basin

Phosphorus is an essential nutrient for life. The release of phosphorus from sediments is critical in sustaining phytoplankton growth in many aquatic systems and is pivotal to eutrophication and the development of bottom water hypoxia. Conventionally, sediment phosphorus release is thought to be controlled by changes in iron oxide reduction driven by variations in external environmental factors, such as organic matter input and bottom water oxygen. Here, we show that internal shifts in microbial communities, and specifically the population dynamics of cable bacteria, can also induce strong seasonality in sedimentary iron-phosphorus dynamics. Field observations in a seasonally hypoxic coastal basin demonstrate that the long-range electrogenic metabolism of cable bacteria leads to a dissolution of iron sulfides in winter and spring. Subsequent oxidation of the mobilized ferrous iron with manganese oxides results in a large stock of iron-oxide-bound phosphorus below the oxic zone. In summer, when bottom water hypoxia develops and cable bacteria are undetectable, the phosphorus associated with these iron oxides is released, strongly increasing phosphorus availability in the water column. Future research should elucidate whether formation of iron-oxide-bound phosphorus driven by cable bacteria, as observed in this study, contributes to the seasonality in iron-phosphorus cycling in aquatic sediments worldwide.

Pore water and solid-phase measurements on sediment cores from the Black Sea

The surface sediments in the Black Sea are underlain by extensive deposits of iron (Fe) oxide-rich lake sediments that were deposited prior to the inflow of marine Mediterranean Sea waters ca. 9000 years ago. The subsequent downward diffusion of marine sulfate into the methane-bearing lake sediments has led to a multitude of diagenetic reactions in the sulfate-methane transition zone (SMTZ), including anaerobic oxidation of methane (AOM) with sulfate. While the sedimentary cycles of sulfur (S), methane and Fe in the SMTZ have been extensively studied, relatively little is known about the diagenetic alterations of the sediment record occurring below the SMTZ. Here we combine detailed geochemical analyses of the sediment and pore water with multicomponent diagenetic modeling to study the diagenetic alterations below the SMTZ at two sites in the western Black Sea. We focus on the dynamics of Fe, S and phosphorus (P) and demonstrate that diagenesis has strongly overprinted the sedimentary burial records of these elements. Our results show that sulfate-mediated AOM substantially enhances the downward diffusive flux of sulfide into the deep limnic deposits. During this downward sulfidization, Fe oxides, Fe carbonates and Fe phosphates (e.g. vivianite) are converted to sulfide phases, leading to an enrichment in solid phase S and the release of phosphate to the pore water. Below the sulfidization front, high concentrations of dissolved ferrous Fe (Fe2+) lead to sequestration of downward diffusing phosphate as authigenic vivianite, resulting in a transient accumulation of total P directly below the sulfidization front. Our model results further demonstrate that downward migrating sulfide becomes partly re-oxidized to sulfate due to reactions with oxidized Fe minerals, fueling a cryptic S cycle and thus stimulating slow rates of sulfate-driven AOM (~ 1-100 pmol/cm**3/d) in the sulfate-depleted limnic deposits. However, this process is unlikely to explain the observed release of dissolved Fe2+ below the SMTZ. Instead, we suggest that besides organoclastic Fe oxide reduction, AOM coupled to the reduction of Fe oxides may also provide a possible mechanism for the high concentrations of Fe2+ in the pore water at depth. Our results reveal that methane plays a key role in the diagenetic alterations of Fe, S and P records in Black Sea sediments. The downward sulfidization into the limnic deposits is enhanced through sulfate-driven AOM with sulfate and AOM with Fe oxides may provide a deep source of dissolved Fe2+ that drives the sequestration of P in vivianite below the sulfidization front.