Dorina Seitaj

Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor

Recently, a novel mode of sulphur oxidation was described in marine sediments, in which sulphide oxidation in deeper anoxic layers was electrically coupled to oxygen reduction at the sediment surface. Subsequent experimental evidence identified that long filamentous bacteria belonging to the family Desulfobulbaceae likely mediated the electron transport across the centimetre-scale distances. Such long-range electron transfer challenges some long-held views in microbial ecology and could have profound implications for sulphur cycling in marine sediments. But, so far, this process of electrogenic sulphur oxidation has been documented only in laboratory experiments and so its imprint on the seafloor remains unknown. Here we show that the geochemical signature of electrogenic sulphur oxidation occurs in a variety of coastal sediment environments, including a salt marsh, a seasonally hypoxic basin, and a subtidal coastal mud plain. In all cases, electrogenic sulphur oxidation was detected together with an abundance of Desulfobulbaceae filaments. Complementary laboratory experiments in intertidal sands demonstrated that mechanical disturbance by bioturbating fauna destroys the electrogenic sulphur oxidation signal. A survey of published geochemical data and 16S rRNA gene sequences identified that electrogenic sulphide oxidation is likely present in a variety of marine sediments with high sulphide generation and restricted bioturbation, such as mangrove swamps, aquaculture areas, seasonally hypoxic basins, cold sulphide seeps and possibly hydrothermal vent environments. This study shows for the first time that electrogenic sulphur oxidation occurs in a wide range of marine sediments and that bioturbation may exert a dominant control on its natural distribution.

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.

Electrogenic Sulfur Oxidation by Cable Bacteria in Bivalve Reef Sediments

Cable bacteria induce long-distance electron transport in the seafloor and can exert a powerful control on the elemental cycling in marine sediments by creating extreme excursions in porewater pH. Yet, the natural distribution of cable bacteria is still largely unknown, and so their role in coastal biogeochemical cycling remains poorly quantified. Here we show that cable bacteria can be abundant in the sediments of intertidal bivalve reefs, where they strongly influence the pore water geochemistry, resulting in a potentially beneficial interaction between the sulfur oxidizing microbes and biodepositing fauna. Cable bacteria occurred in sediments accumulating within mussel and oyster reefs in the Wadden Sea (The Netherlands), at cumulative filament densities up to 1038 m cm-2. Additionally, cable bacteria were found at moderately high cumulative filament densities (up to 56 m cm-2) in a heavily bioturbated sandy sediment adjacent to the muddy reefs. Microsensor profiling revealed strong sulfide removal and intense acid generation associated with the electrogenic sulfide oxidation metabolism of the cable bacteria. Strongly elevated concentrations of dissolved calcium (up to 35 mM), manganese (up to 250 µM), and iron (up to 700 µM) were observed in the pore waters, consistent with acidity-driven dissolution of calcium carbonates and iron sulfides. This field study provides substantive evidence that cable bacteria exert a decisive control on the cycling of sulfur and carbonate minerals in cohesive coastal sediments, and identifies that the distribution and influence of cable bacteria covers a greater range of natural habitats than previously believed.