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Over the last decades, hypoxia in marine coastal environments has become more and more widespread, prolonged and intense. Hypoxic events have large consequences for the functioning of benthic ecosystems. In severe cases, they may lead to complete anoxia and the presence of toxic sulfides in the sediment and bottom-water, thereby strongly affecting biological compartments of benthic marine ecosystems. Within these ecosystems, benthic foraminifera show a high diversity of ecological responses, with a wide range of adaptive life strategies. Some species are particularly resistant to hypoxia–anoxia, and consequently it is interesting to study the whole foraminiferal community as well as species-specific responses to such events. Here we investigated the temporal dynamics of living benthic foraminiferal communities (recognised by CellTracker™ Green) at two sites in the saltwater Lake Grevelingen in the Netherlands. These sites are subject to seasonal anoxia with different durations and are characterised by the presence of free sulfide (H2S) in the uppermost part of the sediment. Our results indicate that foraminiferal communities are impacted by the presence of H2S in their habitat, with a stronger response in the case of longer exposure times. At the deepest site (34 m), in summer 2012, 1 to 2 months of anoxia and free H2S in the surface sediment resulted in an almost complete disappearance of the foraminiferal community. Conversely, at the shallower site (23 m), where the duration of anoxia and free H2S was shorter (1 month or less), a dense foraminiferal community was found throughout the year except for a short period after the stressful event. Interestingly, at both sites, the foraminiferal community showed a delayed response to the onset of anoxia and free H2S , suggesting that the combination of anoxia and free H2S does not lead to increased mortality, but rather to strongly decreased reproduction rates. At th

Recycling of phosphorus (P) from sediments contributes to the development of bottom-water hypoxia in many coastal systems. Here, we present results of a year-long assessment of P dynamics in sediments of a seasonally hypoxic coastal marine basin (Lake Grevelingen, the Netherlands) in 2012. Sequential phosphorus extractions (SEDEX) and X-ray absorption spectroscopy (XAS) indicate that P was adsorbed to Fe-(III)-(oxyhydr)oxides when cable bacteria were active in the surface sediments in spring. With the onset of summer hypoxia, sulphide-induced dissolution of the Fe-(III)-(oxyhydr)oxides led to P release to the pore water and overlying water. The similarity in authigenic Ca-P concentrations in the sediment and suspended matter suggest that Ca-P is not formed in situ. The P burial efficiency was ≤ 32%. Hypoxia-driven sedimentary P recycling had a major impact on the water-column chemistry in the basin in 2012. Water-column monitoring data indicate up to ninefold higher surface water concentrations of phosphate in the basin in the late 1970s and a stronger hypoxia-driven seasonal P release from the sediment. The amplified release of P from the sediment in the past is attributed to the presence of a larger pool of Fe-bound P in the basin prior to the first onset of hypoxia. Given that P is not limiting, primary production in the basin has not been affected by the decadal changes in P availability and recycling over the past 40 years. The changes in P dynamics on decadal time scales were

Seasonal hypoxia in coastal systems drastically changes the availability of electron acceptors in bottom water, which alters the sedimentary reoxidation of reduced compounds. However, the effect of seasonal hypoxia on the chemolithoautotrophic community that catalyzes these reoxidation reactions is rarely studied. Here, we examine the changes in activity and structure of the sedimentary chemolithoautotrophic bacterial community of a seasonally hypoxic saline basin under oxic (spring) and hypoxic (summer) conditions. Combined 16S rRNA gene amplicon sequencing and analysis of phospholipid-derived fatty acids indicated a major temporal shift in community structure. Aerobic sulfur-oxidizing Gammaproteobacteria (Thiotrichales) and Epsilonproteobacteria (Campylobacterales) were prevalent during spring, whereas Deltaproteobacteria (Desulfobacterales) related to sulfate-reducing bacteria prevailed during summer hypoxia. Chemolithoautotrophy rates in the surface sediment were three times higher in spring than in summer. The depth distribution of chemolithoautotrophy was linked to the distinct sulfur oxidation mechanisms identified through microsensor profiling, i.e., canonical sulfur oxidation, electrogenic sulfur oxidation by cable bacteria, and sulfide oxidation coupled to nitrate reduction by Beggiatoaceae. The metabolic diversity of the sulfur-oxidizing bacterial community suggests a complex niche partitioning within the sediment, probably driven by the availability of reduced sulfur compounds (H2S, S0, and S2O32−) and electron acceptors (O2 and NO3−) regulated by seasonal hypoxia.

Recently, long filamentous bacteria have been reported conducting electrons over centimetre distances in marine sediments. These so-called cable bacteria perform an electrogenic form of sulfur oxidation, whereby long-distance electron transport links sulfide oxidation in deeper sediment horizons to oxygen reduction in the upper millimetres of the sediment. Electrogenic sulfur oxidation exerts a strong impact on the local sediment biogeochemistry, but it is currently unknown how prevalent the process is within the seafloor. Here we provide a state-of-the-art assessment of its global distribution by combining new field observations with previous reports from the literature. This synthesis demonstrates that electrogenic sulfur oxidation, and hence microbial long-distance electron transport, is a widespread phenomenon in the present-day seafloor. The process is found in coastal sediments within different climate zones (off the Netherlands, Greenland, the USA, Australia) and thrives on a range of different coastal habitats (estuaries, salt marshes, mangroves, coastal hypoxic basins, intertidal flats). The combination of a widespread occurrence and a strong local geochemical imprint suggests that electrogenic sulfur oxidation could be an important, and hitherto overlooked, component of the marine cycle of carbon, sulfur and other elements.

Cable bacteria have recently been identified in various sedimentary marine settings worldwide. These filamentous microbes mediate electrogenic sulphur oxidation (e-SOx) over centimetre-scale distances, leading to a distinct separation of oxygen- and sulphide-bearing sediment zones. Here we present results of a year-long monthly assessment of the impact of cable bacteria on sedimentary Fe and Mn dynamics at three sites located along a water depth gradient in a seasonally-hypoxic coastal marine lake (Grevelingen, The Netherlands). Fluorescence In Situ Hybridisation (FISH) shows the presence of cable bacteria at two sites in spring. Micro-sensor profiling (O2, pH, H2S) and pore water profiles of dissolved Mn, Fe2+, Ca2+ and SO42− reveal the geochemical signature of e-SOx at these sites, i.e. the development of a broad suboxic zone, characterised by a low pH and acidic dissolution of Ca/Mn carbonates and Fe sulphides. Cable bacteria activity, as reflected by dissolution of FeS in spring, was highest at the deepest and most hypoxic site. In spring, dissolved Mn and Fe2+ released at depth due to e-SOx diffused upwards and was sequestered as Mn- and Fe-(oxyhydr)oxides near the sediment surface, with Mn oxides acting as an oxidant for part of the upward diffusing Fe2+. Strikingly, the thickness of the Fe-(oxyhydr)oxide-bearing surface layer of the sediment was greatest at the most hypoxic site, emphasising the key role of cable bacteria in creating oxidised surface sediments. X-ray absorption fine structure analyses confirm the seasonality in Fe-(oxyhydr)oxide formation and reveal that the sediment Mn oxides were of biogenic (birnessite) and abiotic (hausmannite) origin. Upon the onset of hypoxia in early summer, the sediment Fe-(oxyhydr)oxides were mostly converted to Fe-sulphides but the Mn oxides dissolved and the Mn was lost to the overlying water. After summer hypoxia, Beggiatoaceae

Phosphorus is an essential nutrient for life. The release ofphosphorus from sediments is critical in sustaining phytoplankton growthin many aquatic systems and is pivotal to eutrophication and thedevelopment of bottom water hypoxia. Conventionally, sedimentphosphorus release is thought to be controlled by changes in iron oxidereduction driven by variations in external environmental factors, such asorganic matter input and bottom water oxygen. Here, we show thatinternal shifts in microbial communities, and specifically the populationdynamics of cable bacteria, can also induce strong seasonality insedimentary iron-phosphorus dynamics. Field observations in a seasonallyhypoxic coastal basin demonstrate that the long-range electrogenicmetabolism of cable bacteria leads to a dissolution of iron sulfides inwinter and spring. Subsequent oxidation of the mobilized ferrous iron withmanganese oxides results in a large stock of iron-oxide-bound phosphorusbelow the oxic zone. In summer, when bottom water hypoxia develops and cable bacteria are undetectable, the phosphorusassociated with these iron oxides is released, strongly increasing phosphorus availability in the water column. Future researchshould 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.

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.

Coastal areas are impacted by multiple natural and anthropogenic processes and experience stronger pH fluctuations than the open ocean. These variations can weaken or intensify the ocean acidification signal induced by increasing atmospheric pCO2. The development of eutrophication-induced hypoxia intensifies coastal acidification, since the CO2 produced during respiration decreases the buffering capacity in any hypoxic bottom water. To assess the combined ecosystem impacts of acidification and hypoxia, we quantified the seasonal variation in pH and oxygen dynamics in the water column of a seasonally stratified coastal basin (Lake Grevelingen, the Netherlands). Monthly water-column chemistry measurements were complemented with estimates of primary production and respiration using O2 light–dark incubations, in addition to sediment–water fluxes of dissolved inorganic carbon (DIC) and total alkalinity (TA). The resulting data set was used to set up a proton budget on a seasonal scale. Temperature-induced seasonal stratification combined with a high community respiration was responsible for the depletion of oxygen in the bottom water in summer. The surface water showed strong seasonal variation in process rates (primary production, CO2 air–sea exchange), but relatively small seasonal pH fluctuations (0.46 units on the total hydrogen ion scale). In contrast, the bottom water showed less seasonality in biogeochemical rates (respiration, sediment–water exchange), but stronger pH fluctuations (0.60 units). This marked difference in pH dynamics could be attributed to a substantial reduction in the acid–base buffering capacity of the hypoxic bottom water in the summer period. Our results highlight the importance of acid–base buffering in the pH dynamics of coastal systems and illustrate the increasing vulnerability of hypoxic, CO2-rich waters to any acidifying process.

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.