Iron Promotes the Retention of Terrigenous Dissolved Organic Matter in Subtidal Permeable Sediments.

Marine permeable sediments are important sites for organic matter turnover in the coastal ocean. However, little is known about their role in trapping dissolved organic matter (DOM). Here, we examined DOM abundance and molecular compositions (9804 formulas identified) in subtidal permeable sediments along a near- to offshore gradient in the German North Sea. With the salinity increasing from 30.1 to 34.6 PSU, the DOM composition in bottom water shifts from relatively higher abundances of aromatic compounds to more highly unsaturated compounds. In the bulk sediment, DOM leached by ultrapure water (UPW) from the solid phase is 54 ± 20 times more abundant than DOM in porewater, with higher H/C ratios and a more terrigenous signature. With 0.5 M HCl, the amount of leached DOM (enriched in aromatic and oxygen-rich compounds) is doubled compared to UPW, mainly due to the dissolution of poorly crystalline Fe phases (e.g., ferrihydrite and Fe monosulfides). This suggests that poorly crystalline Fe phases promote DOM retention in permeable sediments, preferentially terrigenous, and aromatic fractions. Given the intense filtration of seawater through the permeable sediments, we posit that Fe can serve as an important intermediate storage for terrigenous organic matter and potentially accelerate organic matter burial in the coastal ocean.

The Impact of Sea Ice Cover on Microbial Communities in Antarctic Shelf Sediments.

The area around the Antarctic Peninsula (AP) is facing rapid climatic and environmental changes, with so far unknown impacts on the benthic microbial communities of the continental shelves. In this study, we investigated the impact of contrasting sea ice cover on microbial community compositions in surface sediments from five stations along the eastern shelf of the AP using 16S ribosomal RNA (rRNA) gene sequencing. Redox conditions in sediments with long ice-free periods are characterized by a prevailing ferruginous zone, whereas a comparatively broad upper oxic zone is present at the heavily ice-covered station. Low ice cover stations were highly dominated by microbial communities of Desulfobacterota (mostly Sva1033, Desulfobacteria, and Desulfobulbia), Myxococcota, and Sva0485, whereas Gammaproteobacteria, Alphaproteobacteria, Bacteroidota, and NB1-j prevail at the heavy ice cover station. In the ferruginous zone, Sva1033 was the dominant member of Desulfuromonadales for all stations and, along with eleven other taxa, showed significant positive correlations with dissolved Fe concentrations, suggesting a significant role in iron reduction or an ecological relationship with iron reducers. Our results indicate that sea ice cover and its effect on organic carbon fluxes are the major drivers for changes in benthic microbial communities, favoring potential iron reducers at stations with increased organic matter fluxes.

Uniquely low stable iron isotopic signatures in deep marine sediments caused by Rayleigh distillation.

Dissimilatory iron reduction (DIR) is suggested to be one of the earliest forms of microbial respiration. It plays an important role in the biogeochemical cycling of iron in modern and ancient sediments. Since microbial iron cycling is typically accompanied by iron isotope fractionation, stable iron isotopes are used as tracer for biological activity. Here we present iron isotope data for dissolved and sequentially extracted sedimentary iron pools from deep and hot subseafloor sediments retrieved in the Nankai Trough off Japan. Dissolved iron (Fe(II)aq) is isotopically light throughout the ferruginous sediment interval but some samples have exceptionally light isotope values. Such light values have never been reported in natural marine environments and cannot be solely attributed to DIR. We show that the light isotope values are best explained by a Rayleigh distillation model where Fe(II)aq is continuously removed from the pore water by adsorption onto iron (oxyhydr)oxide surfaces. While the microbially mediated Fe(II)aq release has ceased due to an increase in temperature beyond the threshold of mesophilic microorganisms, the abiotic adsorptive Fe(II)aq removal continued, leading to uniquely light isotope values. These findings have important implications for the interpretation of dissolved iron isotope data especially in deep subseafloor sediments.

Alpha radiation from polymetallic nodules and potential health risks from deep-sea mining.

In search for critical elements, polymetallic nodules at the deep abyssal seafloor are targeted for mining operations. Nodules efficiently scavenge and retain several naturally occurring uranium-series radioisotopes, which predominantly emit alpha radiation during decay. Here, we present new data on the activity concentrations of thorium-230, radium-226, and protactinium-231, as well as on the release of radon-222 in and from nodules from the NE Pacific Ocean. In line with abundantly published data from historic studies, we demonstrate that the activity concentrations for several alpha emitters are often higher than 5 Bq g-1 at the surface of the nodules. These observed values can exceed current exemption levels by up to a factor of 1000, and even entire nodules commonly exceed these limits. Exemption levels are in place for naturally occurring radioactive materials (NORM) such as ores and slags, to protect the public and to ensure occupational health and radiation safety. In this context, we discuss three ways of radiation exposure from nodules, including the inhalation or ingestion of nodule fines, the inhalation of radon gas in enclosed spaces and the potential concentration of some radioisotopes during nodule processing. Seen in this light, inappropriate handling of polymetallic nodules poses serious health risks.

The iron "redox battery" in sandy sediments: Its impact on organic matter remineralization and phosphorus cycling.

Permeable sandy sediments cover 50-60 % of the global continental shelf and are important bioreactors that regulate organic matter (OM) turnover and nutrient cycling in the coastal ocean. In sands, the dynamic porewater advection can cause rapid mass transfer and variable redox conditions, thus affecting OM remineralization pathways, as well as the recycling of iron and phosphorus. In this study, North Sea sands were incubated in flow-through reactors (FTRs) to investigate biogeochemical processes under porewater advection and changing redox conditions. We found that the average rate of anaerobic OM remineralization was 12 times lower than the aerobic pathway, and Fe(III) oxyhydroxides were found to be the major electron acceptors during 34 days of anoxic incubation. Reduced Fe accumulated in the solid phase (expressed as Fe(II)) before significant release of Fe2+ into the porewater, and most of the reduced Fe (~96 %) remained in the solid phase throughout the anoxic incubation. Fe(II) retained in the solid phase, either through the formation of authigenic Fe(II)-bearing minerals or adsorption, was easily re-oxidized upon exposure to O2. Excessive P release (apart from OM remineralization) started at the beginning of the anoxic incubation and accelerated after the release of Fe2+ with a constant P/Fe2+ ratio of 0.26. After 34 days of anoxic incubation, porewater was re­oxygenated and > 99 % of released P was coprecipitated through Fe2+ oxidation (so-called "Fe curtain"). Our results demonstrate that Fe(III)/Fe(II) in the solid phase can serve as a relatively immobile and rechargeable "redox battery" under dynamic porewater advection. This Fe "redox battery" is characteristic for permeable sediments and environments with variable redox conditions, making Fe an important player in OM turnover. We also suggest that P liberated before Fe2+ release can escape the "Fe curtain" in surface sediments, thus potentially increasing net benthic P efflux from permeable sediments under variable redox conditions.

Iron and sulfate reduction structure microbial communities in (sub-)Antarctic sediments.

Permanently cold marine sediments are heavily influenced by increased input of iron as a result of accelerated glacial melt, weathering, and erosion. The impact of such environmental changes on microbial communities in coastal sediments is poorly understood. We investigated geochemical parameters that shape microbial community compositions in anoxic surface sediments of four geochemically differing sites (Annenkov Trough, Church Trough, Cumberland Bay, Drygalski Trough) around South Georgia, Southern Ocean. Sulfate reduction prevails in Church Trough and iron reduction at the other sites, correlating with differing local microbial communities. Within the order Desulfuromonadales, the family Sva1033, not previously recognized for being capable of dissimilatory iron reduction, was detected at rather high relative abundances (up to 5%) while other members of Desulfuromonadales were less abundant (<0.6%). We propose that Sva1033 is capable of performing dissimilatory iron reduction in sediment incubations based on RNA stable isotope probing. Sulfate reducers, who maintain a high relative abundance of up to 30% of bacterial 16S rRNA genes at the iron reduction sites, were also active during iron reduction in the incubations. Thus, concurrent sulfate reduction is possibly masked by cryptic sulfur cycling, i.e., reoxidation or precipitation of produced sulfide at a small or undetectable pool size. Our results show the importance of iron and sulfate reduction, indicated by ferrous iron and sulfide, as processes that shape microbial communities and provide evidence for one of Sva1033's metabolic capabilities in permanently cold marine sediments.

Electron Acceptor Availability Shapes Anaerobically Methane Oxidizing Archaea (ANME) Communities in South Georgia Sediments.

Anaerobic methane oxidizing archaea (ANME) mediate anaerobic oxidation of methane (AOM) in marine sediments and are therefore important for controlling atmospheric methane concentrations in the water column and ultimately the atmosphere. Numerous previous studies have revealed that AOM is coupled to the reduction of different electron acceptors such as sulfate, nitrate/nitrite or Fe(III)/Mn(IV). However, the influence of electron acceptor availability on the in situ ANME community composition in sediments remains largely unknown. Here, we investigated the electron acceptor availability and compared the microbial in situ communities of three methane-rich locations offshore the sub-Antarctic island South Georgia, by Illumina sequencing and qPCR of mcrA genes. The methanic zone (MZ) sediments of Royal Trough and Church Trough comprised high sulfide concentrations of up to 4 and 19 mM, respectively. In contrast, those of the Cumberland Bay fjord accounted for relatively high concentrations of dissolved iron (up to 186 µM). Whereas the ANME community in the sulfidic sites Church Trough and Royal Trough mainly comprised members of the ANME-1 clade, the order-level clade "ANME-1-related" (Lever and Teske, 2015) was most abundant in the iron-rich site in Cumberland Bay fjord, indicating that the availability of electron acceptors has a strong selective effect on the ANME community. This study shows that potential electron acceptors for methane oxidation may serve as environmental filters to select for the ANME community composition and adds to a better understanding of the global importance of AOM.

Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures.

Elevated dissolved iron concentrations in the methanic zone are typical geochemical signatures of rapidly accumulating marine sediments. These sediments are often characterized by co-burial of iron oxides with recalcitrant aromatic organic matter of terrigenous origin. Thus far, iron oxides are predicted to either impede organic matter degradation, aiding its preservation, or identified to enhance organic carbon oxidation via direct electron transfer. Here, we investigated the effect of various iron oxide phases with differing crystallinity (magnetite, hematite, and lepidocrocite) during microbial degradation of the aromatic model compound benzoate in methanic sediments. In slurry incubations with magnetite or hematite, concurrent iron reduction, and methanogenesis were stimulated during accelerated benzoate degradation with methanogenesis as the dominant electron sink. In contrast, with lepidocrocite, benzoate degradation, and methanogenesis were inhibited. These observations were reproducible in sediment-free enrichments, even after five successive transfers. Genes involved in the complete degradation of benzoate were identified in multiple metagenome assembled genomes. Four previously unknown benzoate degraders of the genera Thermincola (Peptococcaceae, Firmicutes), Dethiobacter (Syntrophomonadaceae, Firmicutes), Deltaproteobacteria bacteria SG8_13 (Desulfosarcinaceae, Deltaproteobacteria), and Melioribacter (Melioribacteraceae, Chlorobi) were identified from the marine sediment-derived enrichments. Scanning electron microscopy (SEM) and catalyzed reporter deposition fluorescence in situ hybridization (CARD-FISH) images showed the ability of microorganisms to colonize and concurrently reduce magnetite likely stimulated by the observed methanogenic benzoate degradation. These findings explain the possible contribution of organoclastic reduction of iron oxides to the elevated dissolved Fe2+ pool typically observed in methanic zones of rapidly accumulating coastal and continental margin sediments.

Rates and Microbial Players of Iron-Driven Anaerobic Oxidation of Methane in Methanic Marine Sediments.

The flux of methane, a potent greenhouse gas, from the seabed is largely controlled by anaerobic oxidation of methane (AOM) coupled to sulfate reduction (S-AOM) in the sulfate methane transition (SMT). S-AOM is estimated to oxidize 90% of the methane produced in marine sediments and is mediated by a consortium of anaerobic methanotrophic archaea (ANME) and sulfate reducing bacteria. An additional methane sink, i.e., iron oxide coupled AOM (Fe-AOM), has been suggested to be active in the methanic zone of marine sediments. Geochemical signatures below the SMT such as high dissolved iron, low to undetectable sulfate and high methane concentrations, together with the presence of iron oxides are taken as prerequisites for this process. So far, Fe-AOM has neither been proven in marine sediments nor have the governing key microorganisms been identified. Here, using a multidisciplinary approach, we show that Fe-AOM occurs in iron oxide-rich methanic sediments of the Helgoland Mud Area (North Sea). When sulfate reduction was inhibited, different iron oxides facilitated AOM in long-term sediment slurry incubations but manganese oxide did not. Especially magnetite triggered substantial Fe-AOM activity and caused an enrichment of ANME-2a archaea. Methane oxidation rates of 0.095 ± 0.03 nmol cm-3 d-1 attributable to Fe-AOM were obtained in short-term radiotracer experiments. The decoupling of AOM from sulfate reduction in the methanic zone further corroborated that AOM was iron oxide-driven below the SMT. Thus, our findings prove that Fe-AOM occurs in methanic marine sediments containing mineral-bound ferric iron and is a previously overlooked but likely important component in the global methane budget. This process has the potential to sustain microbial life in the deep biosphere.

Temperature Controls Crystalline Iron Oxide Utilization by Microbial Communities in Methanic Ferruginous Marine Sediment Incubations.

Microorganisms can use crystalline iron minerals for iron reduction linked to organic matter degradation or as conduits for direct interspecies electron transfer (mDIET) to syntrophic partners, e.g., methanogens. The environmental conditions that lead either to reduction or conduit use are so far unknown. We investigated microbial community shifts and interactions with crystalline iron minerals (hematite and magnetite) in methanic ferruginous marine sediment incubations during organic matter (glucose) degradation at varying temperatures. Iron reduction rates increased with decreasing temperature from 30°C to 4°C. Both hematite and magnetite facilitated iron reduction at 4°C, demonstrating that microorganisms in the methanic zone of marine sediments can reduce crystalline iron oxides under psychrophilic conditions. Methanogenesis occurred, however, at higher rates with increasing temperature. At 30°C, both hematite and magnetite accelerated methanogenesis onset and maximum process rates. At lower temperatures (10°C and 4°C), hematite could still facilitate methanogenesis but magnetite served more as an electron acceptor for iron reduction than as a conduit. Different temperatures selected for different key microorganisms: at 30°C, members of genus Orenia, Halobacteroidaceae, at 10°C, Photobacterium and the order Clostridiales, and at 4°C Photobacterium and Psychromonas were enriched. Members of the order Desulfuromonadales harboring known dissimilatory iron reducers were also enriched at all temperatures. Our results show that crystalline iron oxides predominant in some natural environments can facilitate electron transfer between microbial communities at psychrophilic temperatures. Furthermore, temperature has a critical role in determining the pathway of crystalline iron oxide utilization in marine sediment shifting from conduction at 30°C to predominantly iron reduction at lower temperatures.

Evidence for a palaeo-subglacial lake on the Antarctic continental shelf.

Subglacial lakes are widespread beneath the Antarctic Ice Sheet but their control on ice-sheet dynamics and their ability to harbour life remain poorly characterized. Here we present evidence for a palaeo-subglacial lake on the Antarctic continental shelf. A distinct sediment facies recovered from a bedrock basin in Pine Island Bay indicates deposition within a low-energy lake environment. Diffusive-advection modelling demonstrates that low chloride concentrations in the pore water of the corresponding sediments can only be explained by initial deposition of this facies in a freshwater setting. These observations indicate that an active subglacial meltwater network, similar to that observed beneath the extant ice sheet, was also active during the last glacial period. It also provides a new framework for refining the exploration of these unique environments.

Microbial Communities and Organic Matter Composition in Surface and Subsurface Sediments of the Helgoland Mud Area, North Sea.

The role of microorganisms in the cycling of sedimentary organic carbon is a crucial one. To better understand relationships between molecular composition of a potentially bioavailable fraction of organic matter and microbial populations, bacterial and archaeal communities were characterized using pyrosequencing-based 16S rRNA gene analysis in surface (top 30 cm) and subsurface/deeper sediments (30-530 cm) of the Helgoland mud area, North Sea. Fourier Transform Ion Cyclotron Resonance Mass Spectrometry (FT-ICR MS) was used to characterize a potentially bioavailable organic matter fraction (hot-water extractable organic matter, WE-OM). Algal polymer-associated microbial populations such as members of the Gammaproteobacteria, Bacteroidetes, and Verrucomicrobia were dominant in surface sediments while members of the Chloroflexi (Dehalococcoidales and candidate order GIF9) and Miscellaneous Crenarchaeota Groups (MCG), both of which are linked to degradation of more recalcitrant, aromatic compounds and detrital proteins, were dominant in subsurface sediments. Microbial populations dominant in subsurface sediments (Chloroflexi, members of MCG, and Thermoplasmata) showed strong correlations to total organic carbon (TOC) content. Changes of WE-OM with sediment depth reveal molecular transformations from oxygen-rich [high oxygen to carbon (O/C), low hydrogen to carbon (H/C) ratios] aromatic compounds and highly unsaturated compounds toward compounds with lower O/C and higher H/C ratios. The observed molecular changes were most pronounced in organic compounds containing only CHO atoms. Our data thus, highlights classes of sedimentary organic compounds that may serve as microbial energy sources in methanic marine subsurface environments.

Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland mud area, North Sea.

Iron reduction in subseafloor sulfate-depleted and methane-rich marine sediments is currently a subject of interest in subsurface geomicrobiology. While iron reduction and microorganisms involved have been well studied in marine surface sediments, little is known about microorganisms responsible for iron reduction in deep methanic sediments. Here, we used quantitative PCR-based 16S rRNA gene copy numbers and pyrosequencing-based relative abundances of bacteria and archaea to investigate covariance between distinct microbial populations and specific geochemical profiles in the top 5 m of sediment cores from the Helgoland mud area, North Sea. We found that gene copy numbers of bacteria and archaea were specifically higher around the peak of dissolved iron in the methanic zone (250-350 cm). The higher copy numbers at these depths were also reflected by the relative sequence abundances of members of the candidate division JS1, methanogenic and Methanohalobium/ANME-3 related archaea. The distribution of these populations was strongly correlated to the profile of pore-water Fe(2+) while that of Desulfobacteraceae corresponded to the pore-water sulfate profile. Furthermore, specific JS1 populations also strongly co-varied with the distribution of Methanosaetaceae in the methanic zone. Our data suggest that the interplay among JS1 bacteria, methanogenic archaea and Methanohalobium/ANME-3-related archaea may be important for iron reduction and methane cycling in deep methanic sediments of the Helgoland mud area and perhaps in other methane-rich depositional environments.

Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities.

Sulfate reduction is a globally important redox process in marine sediments, yet global rates are poorly quantified. We developed an artificial neural network trained with 199 sulfate profiles, constrained with geomorphological and geochemical maps to estimate global sulfate-reduction rate distributions. Globally, 11.3 teramoles of sulfate are reduced yearly (~15% of previous estimates), accounting for the oxidation of 12 to 29% of the organic carbon flux to the sea floor. Combined with global cell distributions in marine sediments, these results indicate a strong contrast in sub-sea-floor prokaryote habitats: In continental margins, global cell numbers in sulfate-depleted sediment exceed those in the overlying sulfate-bearing sediment by one order of magnitude, whereas in the abyss, most life occurs in oxic and/or sulfate-reducing sediments.

Chapter 1. Impacts of the oceans on climate change.

The oceans play a key role in climate regulation especially in part buffering (neutralising) the effects of increasing levels of greenhouse gases in the atmosphere and rising global temperatures. This chapter examines how the regulatory processes performed by the oceans alter as a response to climate change and assesses the extent to which positive feedbacks from the ocean may exacerbate climate change. There is clear evidence for rapid change in the oceans. As the main heat store for the world there has been an accelerating change in sea temperatures over the last few decades, which has contributed to rising sea-level. The oceans are also the main store of carbon dioxide (CO2), and are estimated to have taken up approximately 40% of anthropogenic-sourced CO2 from the atmosphere since the beginning of the industrial revolution. A proportion of the carbon uptake is exported via the four ocean 'carbon pumps' (Solubility, Biological, Continental Shelf and Carbonate Counter) to the deep ocean reservoir. Increases in sea temperature and changing planktonic systems and ocean currents may lead to a reduction in the uptake of CO2 by the ocean; some evidence suggests a suppression of parts of the marine carbon sink is already underway. While the oceans have buffered climate change through the uptake of CO2 produced by fossil fuel burning this has already had an impact on ocean chemistry through ocean acidification and will continue to do so. Feedbacks to climate change from acidification may result from expected impacts on marine organisms (especially corals and calcareous plankton), ecosystems and biogeochemical cycles. The polar regions of the world are showing the most rapid responses to climate change. As a result of a strong ice-ocean influence, small changes in temperature, salinity and ice cover may trigger large and sudden changes in regional climate with potential downstream feedbacks to the climate of the rest of the world. A warming Arctic Ocean may lead to further releases of the potent greenhouse gas methane from hydrates and permafrost. The Southern Ocean plays a critical role in driving, modifying and regulating global climate change via the carbon cycle and through its impact on adjacent Antarctica. The Antarctic Peninsula has shown some of the most rapid rises in atmospheric and oceanic temperature in the world, with an associated retreat of the majority of glaciers. Parts of the West Antarctic ice sheet are deflating rapidly, very likely due to a change in the flux of oceanic heat to the undersides of the floating ice shelves. The final section on modelling feedbacks from the ocean to climate change identifies limitations and priorities for model development and associated observations. Considering the importance of the oceans to climate change and our limited understanding of climate-related ocean processes, our ability to measure the changes that are taking place are conspicuously inadequate. The chapter highlights the need for a comprehensive, adequately funded and globally extensive ocean observing system to be implemented and sustained as a high priority. Unless feedbacks from the oceans to climate change are adequately included in climate change models, it is possible that the mitigation actions needed to stabilise CO2 and limit temperature rise over the next century will be underestimated.

A novel, multi-layered methanotrophic microbial mat system growing on the sediment of the Black Sea.

A novel microbially diverse type of 1- to 5-cm-thick mat performing anaerobic oxidation of methane (AOM) and covering several square metres of the seafloor was discovered in the Black Sea at 180 m water depth. Contrary to other AOM-mat systems of the Black Sea these floating mats are not associated to free gas and are not stabilized by authigenic carbonates. However, supply of methane is ensured by the horizontal orientation of the mats acting as a cover of methane enriched fluids ascending from the underlying sediments. Thorough investigation of their community composition by molecular microbiology and lipid biomarkers, metabolic activities and elemental composition showed that the mats provide a clearly structured system with extracellular polymeric substances (EPS) building the framework of the mats. The top black zone, showing high rates of AOM (15 mumol g(dw) (-1) day(-1)), was dominated by ANME-2, while the following equally active pink layer was dominated by ANME-1 Archaea. The lowest AOM activity (2 mumol g(dw) (-1) day(-1)) and cell numbers were found in the greyish middle part delimited towards the sediment by a second pink, ANME-1-dominated and sometimes a black outer layer (ANME-2). Our work clearly shows that the different microbial populations are established along defined chemical gradients such as methane, sulfate or sulfide.