Volker Brüchert

Detoxification of sulphidic African shelf waters by blooming chemolithotrophs

Coastal waters support ∼90 per cent of global fisheries and are therefore an important food reserve for our planet. Eutrophication of these waters, due to human activity, leads to severe oxygen depletion and the episodic occurrence of hydrogen sulphide—toxic to multi-cellular life—with disastrous consequences for coastal ecosytems. Here we show that an area of ∼7,000 km2 of African shelf, covered by sulphidic water, was detoxified by blooming bacteria that oxidized the biologically harmful sulphide to environmentally harmless colloidal sulphur and sulphate. Combined chemical analyses, stoichiometric modelling, isotopic incubations, comparative 16S ribosomal RNA, functional gene sequence analyses and fluorescence in situ hybridization indicate that the detoxification proceeded by chemolithotrophic oxidation of sulphide with nitrate and was mainly catalysed by two discrete populations of γ- and ε-proteobacteria. Chemolithotrophic bacteria, accounting for ∼20 per cent of the bacterioplankton in sulphidic waters, created a buffer zone between the toxic sulphidic subsurface waters and the oxic surface waters, where fish and other nekton live. This is the first time that large-scale detoxification of sulphidic waters by chemolithotrophs has been observed in an open-ocean system. The data suggest that sulphide can be completely consumed by bacteria in the subsurface waters and, thus, can be overlooked by remote sensing or monitoring of shallow coastal waters. Consequently, sulphidic bottom waters on continental shelves may be more common than previously believed, and could therefore have an important but as yet neglected effect on benthic communities.

A constant flux of diverse thermophilic bacteria into the cold Arctic seabed.

Monitoring Massive Microbial Dispersal Quantifying the relative influence of present-day environmental conditions and geological history on the spatial distribution of species represents a major challenge in microbial ecology. Ecological approaches to distinguish between these two biogeographic controls are limited by environmental variability both in space and through time (see the Perspective by Patterson). Using a 1.5-million-year fossil record of marine diatoms, Cermeño and Falkowski (p. 1539) show that, even at the largest (global) spatial scale, the dispersal of marine diatoms is not very limited. Environmental factors are the primary control shaping the global biogeography of marine diatom morphospecies. Thermophilic microorganisms are routinely detected in permanently cold environments from deep sea sediments to polar soils. Hubert et al. (p. 1541) provide a quantitative analysis of a potentially large-scale dispersion of thermophilic bacteria in the ocean. Approximately 108 thermophilic spores are deposited each year on every square meter of Arctic sediment. Spore-forming bacteria adapted to the hot subsurface biosphere are continually deposited in polar marine sediments. Microorganisms have been repeatedly discovered in environments that do not support their metabolic activity. Identifying and quantifying these misplaced organisms can reveal dispersal mechanisms that shape natural microbial diversity. Using endospore germination experiments, we estimated a stable supply of thermophilic bacteria into permanently cold Arctic marine sediment at a rate exceeding 108 spores per square meter per year. These metabolically and phylogenetically diverse Firmicutes show no detectable activity at cold in situ temperatures but rapidly mineralize organic matter by hydrolysis, fermentation, and sulfate reduction upon induction at 50°C. The closest relatives to these bacteria come from warm subsurface petroleum reservoir and ocean crust ecosystems, suggesting that seabed fluid flow from these environments is delivering thermophiles to the cold ocean. These transport pathways may broadly influence microbial community composition in the marine environment.

Regulation of bacterial sulfate reduction and hydrogen sulfide fluxes in the central Namibian coastal upwelling zone

Abstract The coastal upwelling system off central Namibia is one of the most productive regions of the oceans and is characterized by frequently occurring shelf anoxia with severe effects for the benthic life and fisheries. We present data on water column dissolved oxygen, sulfide, nitrate and nitrite, pore water profiles for dissolved sulfide and sulfate, 35 S-sulfate reduction rates, as well as bacterial counts of large sulfur bacteria from 20 stations across the continental shelf and slope. The stations covered two transects and included the inner shelf with its anoxic and extremely oxygen-depleted bottom waters, the oxygen minimum zone on the continental slope, and the lower continental slope below the oxygen minimum zone. High concentrations of dissolved sulfide, up to 22 mM, in the near-surface sediments of the inner shelf result from extremely high rates of bacterial sulfate reduction and the low capacity to oxidize and trap sulfide. The inner shelf break marks the seaward border of sulfidic bottom waters, and separates two different regimes of bacterial sulfate reduction. In the sulfidic bottom waters on the shelf, up to 55% of sulfide oxidation is mediated by the large nitrate-storing sulfur bacteria, Thiomargarita spp. The filamentous relatives Beggiatoa spp. occupy low-O 2 bottom waters on the outer shelf. Sulfide oxidation on the slope is apparently not mediated by the large sulfur bacteria. The data demonstrate the importance of large sulfur bacteria, which live close to the sediment-water interface and reduce the hydrogen sulfide flux to the water column. Modeling of pore water sulfide concentration profiles indicates that sulfide produced by bacterial sulfate reduction in the uppermost 16 cm of sediment is sufficient to account for the total flux of hydrogen sulfide to the water column. However, the total pool of hydrogen sulfide in the water column is too large to be explained by steady state diffusion across the sediment-water interface. Episodic advection of hydrogen sulfide, possibly triggered by methane eruptions, may contribute to hydrogen sulfide in the water column.

Trophic Structure and Community Stability in an Overfished Ecosystem

Gobbled by Gobies A common feature of overfished marine ecosystems is a tendency for biomass to become dominated by jellyfish and microbes, and for the habitat to become anoxic or hypoxic as large fish species are removed. The Benguela ecosystem off the coast of Namibia is a case in point. Utne-Palm et al. (p. 333) describe how the loss of overfished sardines from the Benguela fishery has provided an opportunity for an endemic fish species, the bearded goby, to exploit jellyfish and microbial biomass and to increase in number. These small fish have in turn become the predominant prey species for the larger fish, birds, and mammals in the region. The significance of the goby lies in its ability to forage on resources traditionally regarded as “dead-ends.” The bearded goby has thus become a key stabilizing component to the turnover of energy in the Benguela ecosystem. An endemic goby exploits jellyfish and microbial biomass, partially restoring the food chain in the Benguela ecosystem. Since the collapse of the pelagic fisheries off southwest Africa in the late 1960s, jellyfish biomass has increased and the structure of the Benguelan fish community has shifted, making the bearded goby (Sufflogobius bibarbatus) the new predominant prey species. Despite increased predation pressure and a harsh environment, the gobies are thriving. Here we show that physiological adaptations and antipredator and foraging behaviors underpin the success of these fish. In particular, body-tissue isotope signatures reveal that gobies consume jellyfish and sulphidic diatomaceous mud, transferring “dead-end” resources back into the food chain.

Controls on stable sulfur isotope fractionation during bacterial sulfate reduction in Arctic sediments

Abstract Sulfur isotope fractionation experiments during bacterial sulfate reduction were performed with recently isolated strains of cold-adapted sulfate-reducing bacteria from Arctic marine sediments with year-round temperatures below 2°C. The bacteria represent quantitatively important members of a high-latitude anaerobic microbial community. In the experiments, cell-specific sulfate reduction rates decreased with decreasing temperature and were only slightly higher than the inferred cell-specific sulfate reduction rates in their natural habitat. The experimentally determined isotopic fractionations varied by less than 5.8‰ with respect to temperature and sulfate reduction rate, whereas the difference in sulfur isotopic fractionation between bacteria with different carbon oxidation pathways was as large as 17.4‰. Incubation of sediment slurries from two Arctic localities across an experimental temperature gradient from −4°C to 39°C yielded an isotopic fractionation of 30‰ below 7.6°C, a fractionation of 14‰ and 15.5‰ between 7.6°C and 25°C, and fractionations of 5‰ and 8‰ above 25°C, respectively. In absence of significant differences in sulfate reduction rates in the high and low temperature range, respectively, we infer that different genera of sulfate-reducing bacteria dominate the sulfate-reducing bacterial community at different temperatures. In the Arctic sediments where these bacteria are abundant the isotopic differences between dissolved sulfate, pyrite, and acid-volatile sulfide are at least twice as large as the experimentally determined isotopic fractionations. On the basis of bacterial abundance and cell-specific sulfate reduction rates, these greater isotopic differences cannot be accounted for by significantly lower in situ bacterial sulfate reduction rates. Therefore, the remaining isotopic difference between sulfate and sulfide must derive from additional isotope effects that exist in the oxidative part of the sedimentary sulfur cycle.

Meiofauna increases bacterial denitrification in marine sediments

Denitrification is a critical process that can alleviate the effects of excessive nitrogen availability in aquatic ecosystems subject to eutrophication. An important part of denitrification occurs in benthic systems where bioturbation by meiofauna (invertebrates <1 mm) and its effect on element cycling are still not well understood. Here we study the quantitative impact of meiofauna populations of different abundance and diversity, in the presence and absence of macrofauna, on nitrate reduction, carbon mineralization and methane fluxes. In sediments with abundant and diverse meiofauna, denitrification is double that in sediments with low meiofauna, suggesting that meiofauna bioturbation has a stimulating effect on nitrifying and denitrifying bacteria. However, high meiofauna densities in the presence of bivalves do not stimulate denitrification, while dissimilatory nitrate reduction to ammonium rate and methane efflux are significantly enhanced. We demonstrate that the ecological interactions between meio-, macrofauna and bacteria are important in regulating nitrogen cycling in soft-sediment ecosystems.

The impact of temperature change on the activity and community composition of sulfate-reducing bacteria in arctic versus temperate marine sediments.

Arctic regions may be particularly sensitive to climate warming and, consequently, rates of carbon mineralization in warming marine sediment may also be affected. Using long-term (24 months) incubation experiments at 0°C, 10°C and 20°C, the temperature response of metabolic activity and community composition of sulfate-reducing bacteria were studied in the permanently cold sediment of north-western Svalbard (Arctic Ocean) and compared with a temperate habitat with seasonally varying temperature (German Bight, North Sea). Short-term (35)S-sulfate tracer incubations in a temperature-gradient block (between -3.5°C and +40°C) were used to assess variations in sulfate reduction rates during the course of the experiment. Warming of arctic sediment resulted in a gradual increase of the temperature optima (T(opt)) for sulfate reduction suggesting a positive selection of psychrotolerant/mesophilic sulfate-reducing bacteria (SRB). However, high rates at in situ temperatures compared with maximum rates showed the predominance of psychrophilic SRB even at high incubation temperatures. Changing apparent activation energies (E(a)) showed that increasing temperatures had an initial negative impact on sulfate reduction that was weaker after prolonged incubations, which could imply an acclimatization response rather than a selection process of the SRB community. The microbial community composition was analysed by targeting the 16S ribosomal RNA using catalysed reporter deposition fluorescence in situ hybridization (CARD-FISH). The results showed the decline of specific groups of SRB and confirmed a strong impact of increasing temperatures on the microbial community composition of arctic sediment. Conversely, in seasonally changing sediment sulfate reduction rates and sulfate-reducing bacterial abundance changed little in response to changing temperature.

Coupled primary production, benthic foraminiferal assemblage, and sulfur diagenesis in organic-rich sediments of the Benguela upwelling system

Abstract Episodically deposited, dark, organic-rich Pleistocene and Late Pliocene sediments from the lower continental slope off southwest Africa reveal complex interactions between changes in primary production, benthic foraminiferal assemblage, and anaerobic microbial processes. The organic-rich layers contain diatom assemblages characteristic of intense seasonal coastal upwelling whereas stratigraphically adjacent sediments reflect pelagic primary production. Coastal upwelling-dominated depositional intervals coincide with periods of enhanced carbon flux to the seafloor. Enhanced organic carbon export during dark layer deposition was accompanied by decreases in the diversity of benthic foraminifera to few opportunistic species adapted to high phytodetritus accumulation rates and low O 2 conditions. In all sediments the sulfur isotopic composition of pyrite indicates redox cycling of sulfide close to the sediment/water interface. The sulfur isotopic evidence and the permanent presence of abundant low O 2 -adapted benthic foraminifera throughout the organic-rich layers suggest an oxygenated benthic environment. Efficient oxidation of sulfide and removal of sulfide by sulfidization of organic matter inhibited buildup of toxic hydrogen sulfide from bacterial sulfate reduction at the sediment/water interface. These data imply that in continental slope sediments underneath productive surface waters benthic dysoxic conditions are maintained by the lateral advection of dissolved oxygen to support a small, but well-adapted benthic community.

Aerobic and anaerobic nitrogen transformation processes in N-2-fixing cyanobacterial aggregates

Colonies of N2-fixing cyanobacteria are key players in supplying new nitrogen to the ocean, but the biological fate of this fixed nitrogen remains poorly constrained. Here, we report on aerobic and anaerobic microbial nitrogen transformation processes that co-occur within millimetre-sized cyanobacterial aggregates (Nodularia spumigena) collected in aerated surface waters in the Baltic Sea. Microelectrode profiles showed steep oxygen gradients inside the aggregates and the potential for nitrous oxide production in the aggregates’ anoxic centres. 15N-isotope labelling experiments and nutrient analyses revealed that N2 fixation, ammonification, nitrification, nitrate reduction to ammonium, denitrification and possibly anaerobic ammonium oxidation (anammox) can co-occur within these consortia. Thus, N. spumigena aggregates are potential sites of nitrogen gain, recycling and loss. Rates of nitrate reduction to ammonium and N2 were limited by low internal nitrification rates and low concentrations of nitrate in the ambient water. Presumably, patterns of N-transformation processes similar to those observed in this study arise also in other phytoplankton colonies, marine snow and fecal pellets. Anoxic microniches, as a pre-condition for anaerobic nitrogen transformations, may occur within large aggregates (⩾1 mm) even when suspended in fully oxygenated waters, whereas anoxia in small aggregates (<1 to ⩾0.1 mm) may only arise in low-oxygenated waters (⩽25 μM). We propose that the net effect of aggregates on nitrogen loss is negligible in NO3−-depleted, fully oxygenated (surface) waters. In NO3−-enriched (>1.5 μM), O2-depleted water layers, for example, in the chemocline of the Baltic Sea or the oceanic mesopelagic zone, aggregates may promote N-recycling and -loss processes.

Anaerobic carbon transformation: Experimental studies with flow-through cells

Using a novel multi-cell continuous flow assembly, we studied the dynamic interactions between high-molecular weight substrate consumption, fermentation, and terminal metabolism by microbial communities in anaerobic marine sediments. This system allowed partial physical separation of individual steps in the remineralization of high-molecular weight organic matter: degradation of high-molecular weight polysaccharides, net formation of volatile fatty acids, and net sulfate reduction. Time series experiments yielded insight into time scales of extracellular enzyme production as well as the onset of terminal metabolism. These data also allowed us to assess the rate dependence of individual steps in organic carbon degradation. The major accumulated product of hydrolysis and fermentation was acetate, followed by lactate and formate. The rate of the initial exoenzymatic hydrolysis of polysaccharides was an order of magnitude faster than fermentation and sulfate reduction rates, and suggested a scenario whereby dissolved organic carbon could at least temporarily accumulate in pore waters. The lag in the consumption of hydrolyzed products by sulfate-reducing bacteria may reflect the differential response of the microbial community to increased substrate availability.