Sulfide Toxicity as Key Control on Anaerobic Oxidation of Methane in Eutrophic Coastal Sediments.

Coastal zones account for 75% of marine methane emissions, despite covering only 15% of the ocean surface area. In these ecosystems, the tight balance between methane production and oxidation in sediments prevents most methane from escaping into seawater. However, anthropogenic activities could disrupt this balance, leading to an increased methane escape from coastal sediments. To quantify and unravel potential mechanisms underlying this disruption, we used a suite of biogeochemical and microbiological analyses to investigate the impact of anthropogenically induced redox shifts on methane cycling in sediments from three sites with contrasting bottom water redox conditions (oxic-hypoxic-euxinic) in the eutrophic Stockholm Archipelago. Our results indicate that the methane production potential increased under hypoxia and euxinia, while anaerobic oxidation of methane was disrupted under euxinia. Experimental, genomic, and biogeochemical data suggest that the virtual disappearance of methane-oxidizing archaea at the euxinic site occurred due to sulfide toxicity. This could explain a near 7-fold increase in the extent of escape of benthic methane at the euxinic site relative to the hypoxic one. In conclusion, these insights reveal how the development of euxinia could disrupt the coastal methane biofilter, potentially leading to increased methane emissions from coastal zones.

Ebullition dominates methane emissions in stratified coastal waters.

Coastal areas are an important source of methane (CH4). However, the exact origins of CH4 in the surface waters of coastal regions, which in turn drive sea-air emissions, remain uncertain. To gain a comprehensive understanding of the current and future climate change feedbacks, it is crucial to identify these CH4 sources and processes that regulate its formation and oxidation. This study investigated coastal CH4 dynamics by comparing water column data from six stations located in the brackish Tvärminne Archipelago, Baltic Sea. The sediment biogeochemistry and microbiology were further investigated at two stations (i.e., nearshore and offshore). These stations differed in terms of stratification, bottom water redox conditions, and organic matter loading. At the nearshore station, CH4 diffusion from the sediment into the water column was negligible, because nearly all CH4 was oxidized within the upper sediment column before reaching the sediment surface. On the other hand, at the offshore station, there was significant benthic diffusion of CH4, albeit the majority underwent oxidation before reaching the sediment-water interface, due to shoaling of the sulfate methane transition zone (SMTZ). The potential contribution of CH4 production in the water column was evaluated and was found to be negligible. After examining the isotopic signatures of δ13C-CH4 across the sediment and water column, it became apparent that the surface water δ13C-CH4 values observed in areas with thermal stratification could not be explained by diffusion, advective fluxes, nor production in the water column. In fact, these values bore a remarkable resemblance to those detected below the SMTZ. This supports the hypothesis that the source of CH4 in surface waters is more likely to originate from ebullition than diffusion in stratified brackish coastal systems.

Cable bacteria regulate sedimentary phosphorus release in freshwater sediments.

Previous studies have demonstrated that e-SOx can regulate the sedimentary release of phosphorus (P) in brackish and marine sediments. When e-SOx is active, an iron (Fe) and manganese (Mn) oxide rich layer is formed near the sediment surface, which prevents P release. When e-SOx becomes inactive, the metal oxide layer is reduced via sulfide-mediated dissolution, and P is subsequently released to the water column. Cable bacteria have been shown to also occur in freshwater sediments. In these sediments, sulfide production is limited, and the metal oxide layer would thus dissolve less efficiently, leaving the P trapped at the sediment surface. This lack of an efficient dissolution mechanism implies that e-SOx could play an important role in the regulation of P availability in eutrophied freshwater streams. To test this hypothesis, we incubated sediments from a eutrophic freshwater river to investigate the impact of cable bacteria on sedimentary cycling of Fe, Mn and P. High-resolution depth profiling of pH, O2 and ΣH2S complemented with FISH analysis and high-throughput gene sequencing showed that the development of e-SOx activity was closely linked to the enrichment of cable bacteria in incubated sediments. Cable bacteria activity caused a strong acidification in the suboxic zone, leading to the dissolution of Fe and Mn minerals and consequently a strong release of dissolved Fe2+ and Mn2+ to the porewater. Oxidation of these mobilized ions at the sediment surface led to the formation of a metal oxide layer that trapped dissolved P, as shown by the enrichment of P-bearing metal oxides in the top layer of the sediment and low phosphate in the pore and overlying water. After e-SOx activity declined, the metal oxide layer did not dissolve and P remained trapped at the surface. Overall, our results suggested cable bacteria can play an important role to counteract eutrophication in freshwater systems.

Coupled dynamics of iron, manganese, and phosphorus in brackish coastal sediments populated by cable bacteria.

Coastal waters worldwide suffer from increased eutrophication and seasonal bottom water hypoxia. Here, we assess the dynamics of iron (Fe), manganese (Mn), and phosphorus (P) in sediments of the eutrophic, brackish Gulf of Finland populated by cable bacteria. At sites where bottom waters are oxic in spring, surface enrichments of Fe and Mn oxides and high abundances of cable bacteria were observed in sediments upon sampling in early summer. At one site, Fe and P were enriched in a thin layer (~ 3 mm) just below the sediment-water interface. X-ray absorption near edge structure and micro X-ray fluorescence analyses indicate that two-thirds of the P in this layer was associated with poorly crystalline Fe oxides, with an additional contribution of Mn(II) phosphates. The Fe enriched layer was directly overlain by a Mn oxide-rich surface layer (~ 2 mm). The Fe oxide layer was likely of diagenetic origin, formed through dissolution of Fe monosulfides and carbonates, potentially induced by cable bacteria in the preceding months when bottom waters were oxic. Most of the Mn oxides were likely deposited from the water column as part of a cycle of repeated deposition and remobilization. Further research is required to confirm whether cable bacteria activity in spring indeed promotes the formation of distinct layers enriched in Fe, Mn, and P minerals in Gulf of Finland sediments. The temporal variations in biogeochemical cycling in this seasonally hypoxic coastal system, potentially controlled by cable bacteria activity, have little impact on permanent sedimentary Fe, Mn, and P burial.

Iron-Phosphorus Feedbacks Drive Multidecadal Oscillations in Baltic Sea Hypoxia.

Hypoxia has occurred intermittently in the Baltic Sea since the establishment of brackish-water conditions at ∼8,000 years B.P., principally as recurrent hypoxic events during the Holocene Thermal Maximum (HTM) and the Medieval Climate Anomaly (MCA). Sedimentary phosphorus release has been implicated as a key driver of these events, but previous paleoenvironmental reconstructions have lacked the sampling resolution to investigate feedbacks in past iron-phosphorus cycling on short timescales. Here we employ Laser Ablation (LA)-ICP-MS scanning of sediment cores to generate ultra-high resolution geochemical records of past hypoxic events. We show that in-phase multidecadal oscillations in hypoxia intensity and iron-phosphorus cycling occurred throughout these events. Using a box model, we demonstrate that such oscillations were likely driven by instabilities in the dynamics of iron-phosphorus cycling under preindustrial phosphorus loads, and modulated by external climate forcing. Oscillatory behavior could complicate the recovery from hypoxia during future trajectories of external loading reductions.

Abundance and Biogeochemical Impact of Cable Bacteria in Baltic Sea Sediments.

Oxygen depletion in coastal waters may lead to release of toxic sulfide from sediments. Cable bacteria can limit sulfide release by promoting iron oxide formation in sediments. Currently, it is unknown how widespread this phenomenon is. Here, we assess the abundance, activity, and biogeochemical impact of cable bacteria at 12 Baltic Sea sites. Cable bacteria were mostly absent in sediments overlain by anoxic and sulfidic bottom waters, emphasizing their dependence on oxygen or nitrate as electron acceptors. At sites that were temporarily reoxygenated, cable bacterial densities were low. At seasonally hypoxic sites, cable bacterial densities correlated linearly with the supply of sulfide. The highest densities were observed at Gulf of Finland sites with high rates of sulfate reduction. Microelectrode profiles of sulfide, oxygen, and pH indicated low or no in situ cable bacteria activity at all sites. Reactivation occurred within 5 days upon incubation of an intact sediment core from the Gulf of Finland with aerated overlying water. We found no relationship between cable bacterial densities and macrofaunal abundances, salinity, or sediment organic carbon. Our geochemical data suggest that cable bacteria promote conversion of iron monosulfides to iron oxides in the Gulf of Finland in spring, possibly explaining why bottom waters in this highly eutrophic region rarely contain sulfide in summer.