Regulation of oxygen dynamics by transport processes and microbial respiration in sandy sediments

More than 50% of the continental shelves are covered by sandy sediments that are permeable and allow for advective porewater flow. The interaction of small scale bedforms and bottom water currents creates pressure gradients, which pump reactive solutes and particles from bottom waters into the sediment where they stimulate benthic microbial communities. This accelerates benthic mineralization and nutrient turnover. So far, studies have generally assumed that the sediment is immobile, even though continental shelves are a high energy environment. Strong tidal currents and waves regularly mobilize the sea floor leading to changes in its morphology. Little is known about the regulation of solute and particle fluxes within sandy sediments when they are exposed to such variable morpho- and hydrodynamics. This thesis aims to improve our understanding of transport processes in sandy sediments and to identify physical and biological parameters controlling benthic biogeochemical cycling

Microstructure and composition of marine aggregates as co-determinants for vertical particulate organic carbon transfer in the global ocean

Marine aggregates are the vector for biogenically bound carbon and nutrients from the euphotic zone to the interior of the oceans. To improve the representation of this biological carbon pump in the global biogeochemical HAMburg Ocean Carbon Cycle (HAMOCC) model, we implemented a novel Microstructure, Multiscale, Mechanistic, Marine Aggregates in the Global Ocean (M4AGO) sinking scheme. M4AGO explicitly represents the size, microstructure, heterogeneous composition, density and porosity of aggregates and ties ballasting mineral and particulate organic carbon (POC) fluxes together. Additionally, we incorporated temperature-dependent remineralization of POC. We compare M4AGO with the standard HAMOCC version, where POC fluxes follow a Martin curve approach with (i) linearly increasing sinking velocity with depth and (ii) temperature-independent remineralization. Minerals descend separately with a constant speed. In contrast to the standard HAMOCC, M4AGO reproduces the latitudinal pattern of POC transfer efficiency, as recently constrained by Weber et al. (2016). High latitudes show transfer efficiencies of ≈0.25±0.04, and the subtropical gyres show lower values of about 0.10±0.03. In addition to temperature as a driving factor for remineralization, diatom frustule size co-determines POC fluxes in silicifier-dominated ocean regions, while calcium carbonate enhances the aggregate excess density and thus sinking velocity in subtropical gyres. Prescribing rising carbon dioxide (CO2) concentrations in stand-alone runs (without climate feedback), M4AGO alters the regional ocean atmosphere CO2 fluxes compared to the standard model. M4AGO exhibits higher CO2 uptake in the Southern Ocean compared to the standard run, while in subtropical gyres, less CO2 is taken up. Overall, the global oceanic CO2 uptake remains the same. With the explicit representation of measurable aggregate properties, M4AGO can serve as a test bed for evaluating the impact of aggregate-associated processes on global biogeochemical cycles and, in particular, on the biological carbon pump

Ciliary flows in corals ventilate target areas of high photosynthetic oxygen production

Most tropical corals live in symbiosis with Symbiodiniaceae algae whose photosynthetic production of oxygen (O2) may lead to excess O2 in the diffusive boundary layer (DBL) above the coral surface. When flow is low, cilia-induced mixing of the coral DBL is vital to remove excess O2 and prevent oxidative stress that may lead to coral bleaching and mortality. Here, we combined particle image velocimetry using O2-sensitive nanoparticles (sensPIV) with chlorophyll (Chla)-sensitive hyperspectral imaging to visualize the microscale distribution and dynamics of ciliary flows and O2 in the coral DBL in relation to the distribution of Symbiodiniaceae Chla in the tissue of the reef building coral, Porites lutea. Curiously, we found an inverse relation between O2 in the DBL and Chla in the underlying tissue, with patches of high O2 in the DBL above low Chla in the underlying tissue surrounding the polyp mouth areas and pockets of low O2 concentrations in the DBL above high Chla in the coenosarc tissue connecting neighboring polyps. The spatial segregation of Chla and O2 is related to ciliary-induced flows, causing a lateral redistribution of O2 in the DBL. In a 2D transport-reaction model of the coral DBL, we show that the enhanced O2 transport allocates parts of the O2 surplus to areas containing less chla, which minimizes oxidative stress. Cilary flows thus confer a spatially complex mass transfer in the coral DBL, which may play an important role in mitigating oxidative stress and bleaching in corals

Ciliary vortex flows and oxygen dynamics in the coral boundary layer

The exchange of metabolites between environment and coral tissue depends on the flux across the diffusive boundary layer (DBL) surrounding the tissue. Cilia covering the coral tissue have been shown to create vortices that enhance mixing in the DBL in stagnant water. To study the role of cilia under simulated ambient currents, we designed a new light-sheet microscopy based flow chamber setup. Microparticle velocimetry was combined with high-resolution oxygen profiling in the coral Porites lutea under varying current and light conditions with natural and arrested cilia beating. Cilia-generated vortices in the lower DBL mitigated extreme oxygen concentrations close to the tissue surface. Under light and arrested cilia, oxygen surplus at the tissue surface increased to 350 µM above ambient, in contrast to 25 µM under ciliary beating. Oxygen shortage in darkness decreased from 120 µM (cilia arrested) to 86 µM (cilia active) below ambient. Ciliary redistribution of oxygen had no effect on the photosynthetic efficiency of the photosymbionts and overall oxygen flux across the DBL indicating that oxygen production and consumption was not affected. We found that corals actively change their environment and suggest that ciliary flows serve predominantly as a homeostatic control mechanism which may play a crucial role in coral stress response and resilience

The impact of bedform migration on benthic oxygen fluxes

Permeable sediments are found wide spread in river beds and on continental shelves. The transport of these sediments is forced by bottom water currents and leads to the formation of bedforms such as ripples and dunes. The bottom water flow across the bedforms results in pressure gradients that drive pore water flow within the permeable sediment and enhance the supply of reactive substrates for biogeochemical processes. This transport-reaction system has been extensively studied for the case of stationary bedforms, whereas bedform migration—the most ubiquitous form of sediment transport—has been often ignored. To study the impact of sediment transport on pore water flow, we incorporated an empirical model of bedform migration into a numerical transport-reaction model for porous media, using oxygen as reactive solute. The modeled oxygen flux changes significantly as soon as the sediment divides into an upper mobile layer (migrating bedform) and a stationary layer underneath. The bedform is increasingly flushed with oxic bottom water, whereas pressure gradients and pore water flow reverse at increasing rate underneath the bedform. This suppresses net pore water displacement and reduces the oxygen penetration depth up to 90%. In effect, the overall oxygen uptake decreases significantly with bedform migration although bottom water velocities increase. This counterintuitive effect is systematically described for a range of different sediment types, current velocities, and respiration rates and should be considered in future studies

The effect of sediment grain properties and porewater flow on microbial abundance and respiration in permeable sediments

Sandy sediments cover 50–60% of the continental shelves and are highly efficient bioreactors in which organic carbon is remineralized and inorganic nitrogen is reduced to N2. As such they seem to play an important role, buffering the open ocean from anthropogenic nitrogen inputs and likely remineralizing the vast amounts of organic matter formed in the highly productive surface waters. To date however, little is known about the interrelation between porewater transport, grain properties and microbial colonization and the consequences for remineralization rates in sandy sediments. To constrain the effect of theses factors on remineralization in silicate sands, we incubated North Sea sediments in flow-through reactors after separating into five different grain size fractions. Bulk sediment and sediment grain properties were measured along with microbial colonization and cell abundances, oxygen consumption and denitrification rates. Volumetric oxygen consumption ranged from 14 to 77 µmol O2 l−1 h−1 while nitrogen-loss via denitrification was between 3.7 and 8.4 µmol N l−1 h−1. Oxygen consumption and denitrification rates were linearly correlated to the microbial cell abundances, which ranged from 2.9 to 5.4·108 cells cm−3. We found, that cell abundance and consumption rates in sandy sediments are influenced (i) by the surface area available for microbial colonization and (ii) by the exposure of these surfaces to the solute-supplying porewater flow. While protective structures such as cracks and depressions promote microbial colonization, the oxygen demand is only met by good ventilation of these structures, which is supported by a high sphericity of the grains. Based on our results, spherical sand grains with small depressions, i.e. golf ball like structures, provide the optimal supporting mineral structure for microorganisms on continental shelves

Regulation of benthic oxygen fluxes in permeable sediments of the coastal ocean

Large areas of the oceanic shelf are composed of sandy sediments through which reactive solutes are transported via porewater advection fueling active microbial communities. The advective oxygen transport in permeable sands of the North Sea was investigated under in situ conditions using a new benthic observatory to assess the dynamic interaction of hydrodynamics, sediment morphodynamics, and oxygen penetration depth. During 16 deployments, concurrent measurement of current velocity, sediment topography, and porewater oxygen concentration were carried out. In all cases the oxyclines were found at depths of 1–6 cm, correlating with the topography of stationary and migrating bedforms (ripples). Different conditions in terms of bottom water currents and bedform migration led to fluctuating oxygen penetration depths and, hence, highly variable redox conditions in up to 2.5 cm thick layers beneath the surface. Volumetric oxygen consumption rates of surface sediments were measured on board in flow-through reactors. Bedform migration was found to reduce consumption rates by up to 50%, presumably caused by the washout of organic carbon that is otherwise trapped in the pore space of the sediment. Based on the observations we found oxygen penetration depths to be largely controlled by oxygen consumption rates, grain size, and current velocity. These controlling variables are summarized by an adapted Damköhler number which allows for prediction of oxygen penetretion depths based on a simple scaling law. By integrating the oxygen consumption rates over the oxygen penetration depth, oxygen fluxes of 8–34 mmol m−2 d−1 were estimate

Impact of shallow‐water hydrothermal seepage on benthic biogeochemical cycling, nutrient availability, and meiobenthic communities in a tropical coral reef

We investigated the influence of high-CO2 hydrothermal seepage on element cycling, early diagenetic processes, and meiobenthic communities in sediments of a coral reef in Papua New Guinea. Based on fluid flow velocities, determined from temperature gradients, and element concentrations, the solute fluxes from the seeps were estimated, showing that seepage through sediments can be a source of nutrients but also of potentially toxic elements to the reef ecosystem. The sediment pore waters consisted of up to 36% hydrothermal fluids, enriched in As, Si, Li, Mn, Fe, Rb, and Cs relative to ambient seawater. During their ascent to the seabed, the acidic fluids reacted with the sediments, leading to increases in total alkalinity, nutrients, and alkali elements in the fluids. Mixing of hydrothermal fluids with seawater within the sediments lead to precipitation of redox-reactive species, including Fe-oxides, but the sediment pore waters were still a source of trace metals to the water column. Presence of the low-pH fluids in the sediments resulted in dissolution of sedimentary carbonates and left behind finer-grained volcanoclastic sands containing As, Cr, and Ni in concentrations toxic to biota. These finer-grained sediments had a reduced permeability, reducing the rate of remineralization of organic matter. Benthic meiofauna and nematode abundance and functional diversity were relatively lower at sites with hydrothermal seepage through the sediment. As benthic and pelagic processes are tightly coupled, it is likely that the changes in benthic biogeochemical processes due to sediment acidification will also affect epibenthic and pelagic communities

Diverse methylotrophic methanogenic archaea cause high methane emissions from seagrass meadows

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Schorn, S., Ahmerkamp, S., Bullock, E., Weber, M., Lott, C., Liebeke, M., Lavik, G., Kuypers, M. M. M., Graf, J. S., & Milucka, J. Diverse methylotrophic methanogenic archaea cause high methane emissions from seagrass meadows. Proceedings of the National Academy of Sciences of the United States of America, 119(9), (2022): e2106628119, https://doi.org/10.1073/pnas.2106628119.Marine coastlines colonized by seagrasses are a net source of methane to the atmosphere. However, methane emissions from these environments are still poorly constrained, and the underlying processes and responsible microorganisms remain largely unknown. Here, we investigated methane turnover in seagrass meadows of Posidonia oceanica in the Mediterranean Sea. The underlying sediments exhibited median net fluxes of methane into the water column of ca. 106 µmol CH4 ⋅ m−2 ⋅ d−1. Our data show that this methane production was sustained by methylated compounds produced by the plant, rather than by fermentation of buried organic carbon. Interestingly, methane production was maintained long after the living plant died off, likely due to the persistence of methylated compounds, such as choline, betaines, and dimethylsulfoniopropionate, in detached plant leaves and rhizomes. We recovered multiple mcrA gene sequences, encoding for methyl-coenzyme M reductase (Mcr), the key methanogenic enzyme, from the seagrass sediments. Most retrieved mcrA gene sequences were affiliated with a clade of divergent Mcr and belonged to the uncultured Candidatus Helarchaeota of the Asgard superphylum, suggesting a possible involvement of these divergent Mcr in methane metabolism. Taken together, our findings identify the mechanisms controlling methane emissions from these important blue carbon ecosystems.This project was funded by theMax Planck Society