A Cross-System Comparison of Dark Carbon Fixation in Coastal Sediments

Dark carbon fixation (DCF) by chemoautotrophic microorganisms can sustain food webs in the seafloor by local production of organic matter independent of photosynthesis. The process has received considerable attention in deep sea systems, such as hydrothermal vents, but the regulation, depth distribution, and global importance of coastal sedimentary DCF have not been systematically investigated. Here we surveyed eight coastal sediments by means of stable isotope probing (13C-DIC) combined with bacterial biomarkers (phospholipid-derived fatty acids) and compiled additional rates from literature into a global database. DCF rates in coastal sediments range from 0.07 to 36.30 mmol C m−2 day−1, and there is a linear relation between DCF and water depth. The CO2 fixation ratio (DCF/CO2 respired) also shows a trend with water depth, decreasing from 0.09 in nearshore environments to 0.04 in continental shelf sediments. Five types of depth distributions of chemoautotrophic activity are identified based on the mode of pore water transport (advective, bioturbated, and diffusive) and the dominant pathway of microbial sulfur oxidation. Extrapolated to the global coastal ocean, we estimate a DCF rate of 0.04 to 0.06 Pg C year−1, which is less than previous estimates based on indirect measurements (0.15 Pg C year−1), but remains substantially higher than the global DCF rate at deep sea hydrothermal vents (0.001–0.002 Pg C year−1).BT/Environmental Biotechnolog

Quantification of Cable Bacteria in Marine Sediments via qPCR

Cable bacteria (Deltaproteobacteria, Desulfobulbaceae) are long filamentous sulfur-oxidizing bacteria that generate long-distance electric currents running through the bacterial filaments. This way, they couple the oxidation of sulfide in deeper sediment layers to the reduction of oxygen or nitrate near the sediment-water interface. Cable bacteria are found in a wide range of aquatic sediments, but an accurate procedure to assess their abundance is lacking. We developed a qPCR approach that quantifies cable bacteria in relation to other bacteria within the family Desulfobulbaceae. Primer sets targeting cable bacteria, Desulfobulbaceae and the total bacterial community were applied in qPCR with DNA extracted from marine sediment incubations. Amplicon sequencing of the 16S rRNA gene V4 region confirmed that cable bacteria were accurately enumerated by qPCR, and suggested novel diversity of cable bacteria. The conjoint quantification of current densities and cell densities revealed that individual filaments carry a mean current of ∼110 pA and have a cell specific oxygen consumption rate of 69 fmol O2 cell–1 day–1. Overall, the qPCR method enables a better quantitative assessment of cable bacteria abundance, providing new metabolic insights at filament and cell level, and improving our understanding of the microbial ecology of electrogenic sediments.BT/Environmental Biotechnolog

Biogeochemical impact of cable bacteria on coastal Black Sea sediment

Cable bacteria can strongly alter sediment biogeochemistry. Here, we used laboratory incubations to determine the potential impact of their activity on the cycling of iron (Fe), phosphorus (P) and sulfur (S). Microsensor depth profiles of oxygen, sulfide and pH in combination with electric potential profiling and fluorescence in situ hybridisation (FISH) analyses showed a rapid development (5 d) of cable bacteria, followed by a long period of activity (200 d). During most of the experiment, the current density correlated linearly with the oxygen demand. Sediment oxygen uptake was attributed to the activity of cable bacteria and the oxidation of reduced products from the anaerobic degradation of organic matter, such as ammonium. Pore water sulfide was low (5 uM) throughout the experiment. Sulfate reduction acted as the main source of sulfide for cable bacteria. Pore water Fe2C reached levels of up to 1.7mM during the incubations, due to the dissolution of FeS (30 %) and siderite, an Fe carbonate mineral (70 %). Following the upward diffusion of Fe2C, a surface enrichment of Fe oxides formed. Hence, besides FeS, siderite may act as a major source of Fe for Fe oxides in coastal surface sediments where cable bacteria are active. Using uXRF, we show that the enrichments in Fe oxides induced by cable bacteria are located in a thin subsurface layer of 0.3 mm. We show that similar subsurface layers enriched in Fe and P are also observed at field sites where cable bacteria were recently active and little bioturbation occurs. This suggests that such subsurface Fe oxide layers, which are not always visible to the naked eye, could potentially be a marker for recent activity of cable bacteria.BT/Environmental Biotechnolog

The impact of street canyon morphology and traffic volume on NO₂ values in the street canyons of Antwerp

Air pollution remains a major environmental and health concern in urban environments, especially in street canyons that show increased pollution levels due to a lack of natural ventilation. Previous studies have investigated the relationship between street canyon morphology and in-canyon pollution levels. However, these studies are typically limited to the scale of a single street canyon and city-wide assessments on this matter are scarce. In 2018, NO2 concentrations were measured in 321 street canyons in the city of Antwerp (Belgium) as part of the large-scale citizen-science project “CurieuzeNeuzen”. In our research, this data was used to study the correlation between morphological indices (e.g. aspect ratio (AR), lateral aspect ratio (LAR), presence of trees) and the traffic volumes on a city-wide scale. The maximum hourly traffic volume (TVmax) and AR correlated significantly with the measured NO2 values, making them useful indicators for air quality in street canyons. For street canyons with AR > 0.65, a TVmax of 300 vehicles/hour was found as a threshold value to guarantee acceptable air quality. No significant correlations were found for the other parameters. Finally, a number of typical street canyon types were defined, which can be of fundamental interest for further research and spatial policy making.BT/Environmental Biotechnolog

Bistability in the redox chemistry of sediments and oceans

For most of Earth's history, the ocean's interior was pervasively anoxic and showed occasional shifts in ocean redox chemistry between iron-buffered and sulfide-buffered states. These redox transitions are most often explained by large changes in external inputs, such as a strongly altered delivery of iron and sulfate to the ocean, or major shifts in marine productivity. Here, we propose that redox shifts can also arise from small perturbations that are amplified by nonlinear positive feedbacks within the internal iron and sulfur cycling of the ocean. Combining observational evidence with biogeochemical modeling, we show that both sedimentary and aquatic systems display intrinsic iron-sulfur bistability, which is tightly linked to the formation of reduced iron-sulfide minerals. The possibility of tipping points in the redox state of sediments and oceans, which allow large and nonreversible geochemical shifts to arise from relatively small changes in organic carbon input, has important implications for the interpretation of the geological rock record and the causes and consequences of major evolutionary transitions in the history of Earth's biosphere.BT/Environmental Biotechnolog

The impact of scrubber discharge on the water quality in estuaries and ports

Background: The International Maritime Organization (IMO) has set limits on sulphur content in fuels for marine transport. However, vessels continue to use these residual high-sulphur fuels in combination with exhaust gas cleaning systems (EGCS or scrubbers). Next to high sulphur, combustion of these fuels also results in higher emissions of contaminants including metals and PAHs. In scrubbers, exhaust gases are sprayed with water in order to remove SOx, resulting in acidic washwater with elevated contaminant concentrations discharged in the aquatic ecosystem. The number of vessels with scrubbers is increasing rapidly, but knowledge on washwater quality and impact are limited. Results: The scrubber washwater is found to be acidic with elevated concentrations of, e.g. zinc, vanadium, copper, nickel, phenanthrene, naphthalene, fluorene and fluoranthene. Model calculations on the effects of scrubber discharge under scenario HIGH (20% of vessels, 90th percentile concentrations) on the water quality in harbour docks showed a decrease in pH of 0.015 units and an increase in surface water concentrations for e.g. naphthalene (189% increase) and vanadium (46% increase). Conclusions: The IMO established sulphur regulations to mitigate the impact of high sulphur emissions of the maritime sector. However, the use of open-loop scrubbers as an abatement technology will not reduce their contribution to ocean acidification. In addition, different types of scrubbers discharge washwater that is acutely toxic for aquatic organisms. However, washwater is diluted and the compounds for which a large increase in surface water concentrations was calculated in the Antwerp (Belgium) harbour docks (naphthalene > phenanthrene > fluorene > acenaphthene > vanadium) were not the compounds that already exceed their respective Water Quality Standards (WQS). Nevertheless, the WQS of several ‘priority hazardous substances’ (Water Framework Directive) are already exceeded in the docks and the Scheldt estuary. Since these hazardous substances are also identified in the washwater, scrubber washwater discharge should be discouraged in coastal waters and estuaries with large ecological value.BT/Environmental Biotechnolog

Cable bacteria delay euxinia and modulate phosphorus release in coastal hypoxic systems

Cable bacteria are long, filamentous bacteria with a unique metabolism involving centimetre-scale electron transport. They are widespread in the sediment of seasonally hypoxic systems and their metabolic activity stimulates the dissolution of iron sulfides (FeS), releasing large quantities of ferrous iron (Fe2+) into the pore water. Upon contact with oxygen, Fe2+ oxidation forms a layer of iron(oxyhydr)oxides (FeOx), which in its turn can oxidize free sulfide (H2S) and trap phosphorus (P) diffusing upward. The metabolism of cable bacteria could thus prevent the release of H2S from the sediment and reduce the risk of euxinia, while at the same time modulating P release over seasonal timescales. However, experimental support for this so-called ‘iron firewall hypothesis’ is scarce. Here, we collected natural sediment in a seasonally hypoxic basin in three different seasons. Undisturbed sediment cores were incubated under anoxic conditions and the effluxes of H2S, dissolved iron (dFe) and phosphate (PO43−) were monitored for up to 140 days. Cores with recent cable bacterial activity revealed a high stock of sedimentary FeOx, which delayed the efflux of H2S for up to 102 days. Our results demonstrate that the iron firewall mechanism could exert an important control on the prevalence of euxinia and regulate the P release in coastal oceans.BT/Environmental Biotechnolog

Mineral formation induced by cable bacteria performing long-distance electron transport in marine sediments

Cable bacteria are multicellular, filamentous microorganisms that are capable of transporting electrons over centimeter-scale distances. Although recently discovered, these bacteria appear to be widely present in the seafloor, and when active they exert a strong imprint on the local geochemistry. In particular, their electrogenic metabolism induces unusually strong pH excursions in aquatic sediments, which induces considerable mineral dissolution, and subsequent mineral reprecipitation. However, at present, it is unknown whether and how cable bacteria play an active or direct role in the mineral reprecipitation process. To this end we present an explorative study of the formation of sedimentary minerals in and near filamentous cable bacteria using a combined approach of electron microscopy and spectroscopic techniques. Our observations reveal the formation of polyphosphate granules within the cells and two different types of biomineral formation directly associated with multicellular filaments of these cable bacteria: (i) the attachment and incorporation of clay particles in a coating surrounding the bacteria and (ii) encrustation of the cell envelope by iron minerals. These findings suggest a complex interaction between cable bacteria and the surrounding sediment matrix, and a substantial imprint of the electrogenic metabolism on mineral diagenesis and sedimentary biogeochemical cycling. In particular, the encrustation process leaves many open questions for further research. For example, we hypothesize that the complete encrustation of filaments might create a diffusion barrier and negatively impact the metabolism of the cable bacteria.OLD BT/Cell Systems EngineeringBT/Environmental Biotechnolog

A model analysis of centimeter-long electron transport in cable bacteria

The recent discovery of cable bacteria has greatly expanded the known length scale of biological electron transport, as these multi-cellular bacteria are capable of mediating electrical currents across centimeter-scale distances. To enable such long-range conduction, cable bacteria embed a network of regularly spaced, parallel protein fibers in their cell envelope. These fibers exhibit extraordinary electrical properties for a biological material, including an electrical conductivity that can exceed 100 S cm −1. Traditionally, long-range electron transport through proteins is described as a multi-step hopping process, in which the individual hopping steps are described by Marcus electron transport theory. Here, we investigate to what extent such a classical hopping model can explain the conductance data recorded for individual cable bacterium filaments. To this end, the conductive fiber network in cable bacteria is modelled as a set of parallel one-dimensional hopping chains. Comparison of model simulated and experimental current(I)/voltage(V) curves, reveals that the charge transport is field-driven rather than concentration-driven, and there is no significant injection barrier between electrodes and filaments. However, the observed high conductivity levels (>100 S cm −1) can only be reproduced, if we include much longer hopping distances (a > 10 nm) and lower reorganisation energies (λ < 0.2 eV) than conventionally used in electron relay models of protein structures. Overall, our model analysis suggests that the conduction mechanism in cable bacteria is markedly distinct from other known forms of long-range biological electron transport, such as in multi-heme cytochromes.BT/Environmental BiotechnologyQN/Blanter GroupQN/van der Zant La

Cable Bacteria Activity Modulates Arsenic Release From Sediments in a Seasonally Hypoxic Marine Basin

Eutrophication and global change are increasing the occurrence of seasonal hypoxia (bottom-water oxygen concentration <63 μM) in coastal systems worldwide. In extreme cases, the bottom water can become completely anoxic, allowing sulfide to escape from the sediments and leading to the development of bottom-water euxinia. In seasonally hypoxic coastal basins, electrogenic sulfur oxidation by long, filamentous cable bacteria has been shown to stimulate the formation of an iron oxide layer near the sediment-water interface, while the bottom waters are oxygenated. Upon the development of bottom-water anoxia, this iron oxide “firewall” prevents the sedimentary release of sulfide. Iron oxides also act as an adsorption trap for elements such as arsenic. Arsenic is a toxic trace metal, and its release from sediments can have a negative impact on marine ecosystems. Yet, it is currently unknown how electrogenic sulfur oxidation impacts arsenic cycling in seasonally hypoxic basins. In this study, we presented results from a seasonal field study of an uncontaminated marine lake, complemented with a long-term sediment core incubation experiment, which reveals that cable bacteria have a strong impact on the arsenic cycle in a seasonally hypoxic system. Electrogenic sulfur oxidation significantly modulates the arsenic fluxes over a seasonal time scale by enriching arsenic in the iron oxide layer near the sediment-water interface in the oxic period and pulse-releasing arsenic during the anoxic period. Fluxes as large as 20 μmol m−2 day−1 were measured, which are comparable to As fluxes reported from highly contaminated sediments. Since cable bacteria are recognized as active components of the microbial community in seasonally hypoxic systems worldwide, this seasonal amplification of arsenic fluxes is likely a widespread phenomenon.BT/Environmental Biotechnolog