Cryptic Sulfur Cycling Aerobic bacteria and ocean circulation patterns control the formation and distribution of oxygen-minimum zones at moderate depth in the oceans. These habitats host microorganisms that thrive on other metabolic substrates in the absence of oxygen—most commonly, metabolizing thermodynamically favorable nitrogen compounds like nitrate. Off the coast of Chile, however, Canfield et al. (p. 1375 , published online 11 November; see the Perspective by Teske ) suggest that bacteria may often reduce sulfate as well. Metagenomic sequencing revealed the presence of both sulfate-reducing and sulfide-oxidizing bacteria. With the coincidence of sulfate and nitrate reduction, the sulfur and nitrogen cycles may be intimately linked; for example, sulfate reduction could provide nitrogen-rich ammonium for bacteria that ultimately transform it into nitrogen gas.
A major percentage (20 to 40%) of global marine fixed-nitrogen loss occurs in oxygen minimum zones (OMZs). Concentrations of O2 and the sensitivity of the anaerobic N2-producing processes of anammox and denitrification determine where this loss occurs. We studied experimentally how O2 at nanomolar levels affects anammox and denitrification rates and the transcription of nitrogen cycle genes in the anoxic OMZ off Chile. Rates of anammox and denitrification were reversibly suppressed, most likely at the enzyme level. Fifty percent inhibition of N2 and N2O production by denitrification was achieved at 205 and 297 nM O2, respectively, whereas anammox was 50% inhibited at 886 nM O2. Coupled metatranscriptomic analysis revealed that transcripts encoding nitrous oxide reductase (nosZ), nitrite reductase (nirS), and nitric oxide reductase (norB) decreased in relative abundance above 200 nM O2. This O2 concentration did not suppress the transcription of other dissimilatory nitrogen cycle genes, including nitrate reductase (narG), hydrazine oxidoreductase (hzo), and nitrite reductase (nirK). However, taxonomic characterization of transcripts suggested inhibition of narG transcription in gammaproteobacteria, whereas the transcription of anammox narG, whose gene product is likely used to oxidatively replenish electrons for carbon fixation, was not inhibited. The taxonomic composition of transcripts differed among denitrification enzymes, suggesting that distinct groups of microorganisms mediate different steps of denitrification. Sulfide addition (1 µM) did not affect anammox or O2 inhibition kinetics but strongly stimulated N2O production by denitrification. These results identify new O2 thresholds for delimiting marine nitrogen loss and highlight the utility of integrating biogeochemical and metatranscriptomic analyses.
Removal of fixed nitrogen in the water column of the eastern Gotland Basin, central Baltic Sea, was studied during two cruises in September 2008 and August 2010. The water column was stratified with anoxic sulfidic bottom water meeting oxic nitrate containing water at the oxic-anoxic interface. Anammox was never detected whereas denitrification was found in all incubations from anoxic depths and occurred immediately below the oxic-anoxic interface. Sulfide (H 2 S + HS À + S 2À ) was in most cases the only electron donor for denitrification but, in contrast to previous findings, denitrification was in some situations driven by organic matter alone. Nitrous oxide (N 2 O) became an increasingly important product of denitrification with increasing sulfide concentration and was >80% of the total N gas formation at 10 lM sulfide. The potential rates of denitrification measured in incubations at elevated NO À 3 or sulfide concentrations were converted to in situ rates using the measured water column concentrations of NO À 3 and sulfide and the actual measured relations between NO À 3 and sulfide concentrations and denitrification rates. In situ denitrification ranged from 0.24 to 15.9 nM N 2 h À1 . Assuming that these rates were valid throughout the anoxic NO À 3 containing zone, depth integrated in situ denitrification rates of 0.06-2.11 mmol N m À2 d À1 were estimated. The thickness of this zone was generally 3-6 m, which is probably what can be maintained through regular turbulent mixing induced by internal waves at the oxic-anoxic interface. However, layers of up to 55 m thickness with low O 2 water (<10 lM) were observed which was probably the result of larger scale mixing. In such a layer nitrification may produce NO À 3 and once the O 2 has been depleted denitrification will follow resulting in enormous rates per unit area. Even with an active denitrification layer of 3-6 m thickness the pelagic denitrification per unit area clearly exceeded sediment denitrification rates elsewhere in the Baltic Sea. When extrapolated to the entire Baltic Proper (BP) denitrification in the water column was in the range of 132-547 kton N yr À1 and was thus at least as important as sediment denitrification which has recently been estimated to 191 kton N yr À1 . With a total external N-input of 773 kton N yr À1 it is clear that denitrification plays a significant role in the N-budget of the BP.
We quantified the fate and transport of watershed-derived ammonium in a tidal freshwater marsh fringing the nutrientrich Scheldt River in a whole-ecosystem 15 N labeling experiment. 15 N-NH was added to the floodwater entering a 3,477 ϩ 4 m 2 tidal marsh area, and marsh ammonium processing and retention were traced in six subsequent tide cycles. We present data for the water phase components of the marsh system, in which changes in concentration and isotopic enrichment of NO , NO , N 2 O, N 2 , NH , and suspended particulate nitrogen (SPN) were measured in concert with a mass balancestudy. Simultaneous addition of a conservative tracer (NaBr) confirmed that tracer was evenly distributed, and the Br Ϫ budget was almost closed (115% recovery). All analyzed dissolved and suspended N pools were labeled, and 31% of added for 30% of 15 N-transformation. In situ whole-ecosystem nitrification rates were four to nine times higher than those in the water column alone, implying a crucial role for the large reactive marsh surface area in N-transformation. Under conditions of low oxygen concentrations and high ammonium availability, nitrifiers produced N 2 O. Our results show that tidal freshwater marshes function not only as nutrient sinks but also as nutrient transformers.
In a 2.5-year-long environmental engineering experiment in the By Fjord, surface water was pumped into the deepwater where the frequency of deepwater renewals increased by a factor of 10. During the experiment, the deepwater became long-term oxic, and nitrate became the dominating dissolved inorganic nitrogen component. The amount of phosphate in the water column decreased by a factor of 5 due to the increase in flushing and reduction in the leakage of phosphate from the sediments when the sediment surface became oxidized. Oxygenation of the sediments did not increase the leakage of toxic metals and organic pollutants. The bacterial community was the first to show changes after the oxygenation, with aerobic bacteria also thriving in the deepwater. The earlier azoic deepwater bottom sediments were colonized by animals. No structural difference between the phytoplankton communities in the By Fjord and the adjacent Havsten Fjord, with oxygenated deepwater, could be detected during the experiment.Electronic supplementary materialThe online version of this article (doi:10.1007/s13280-014-0524-9) contains supplementary material, which is available to authorized users.
We investigated anammox, denitrification and dissimilatory reduction of nitrite to ammonium (DNRA) activity in the Eastern Tropical South Pacific oxygen minimum zone (OMZ) off northern Chile, at high-depth resolution through the oxycline into the anoxic OMZ core. This was accompanied by high-resolution nutrient and oxygen profiles to link changes in nitrogen transformation rates to physicochemical characteristics of the water column. Denitrification was detected at most depths, but anammox was the most active N2 -producing process, while DNRA was not detectable. Anammox and denitrification were mainly active in the anoxic OMZ core while activity was low to not detectable in the oxycline, except in association with an intrusion of OMZ core water. This indicates that continuous exposure to even submicromolar oxygen levels inhibits the processes either directly or through nitrite limitation. Anammox activity did not peak at the oxic-anoxic boundary but 20-50 m below matching the salinity maximum of the Equatorial Subsurface Water. This suggests that water history plays a major role for anammox activity possibly due to slow growth of anammox bacteria. Denitrification peaked deeper than anammox, likely reflecting a shift in the balance between this process and nitrate reduction to nitrite, governed by the relative availability of nitrate and nitrite.
Ninety per cent of marine organic matter burial occurs in continental margin sediments, where a substantial fraction of organic carbon escapes oxidation and enters long-term geologic storage within sedimentary rocks. In such environments, microbial metabolism is limited by the diffusive supply of electron acceptors. One strategy to optimize energy yields in a resource-limited habitat is symbiotic metabolite exchange among microbial associations. Thermodynamic and geochemical considerations indicate that microbial co-metabolisms are likely to play a critical part in sedimentary organic carbon cycling. Yet only one association, between methanotrophic archaea and sulphate-reducing bacteria, has been demonstrated in marine sediments in situ, and little is known of the role of microbial symbiotic interactions in other sedimentary biogeochemical cycles. Here we report in situ molecular and incubation-based evidence for a novel symbiotic consortium between two chemolithotrophic bacteria--anaerobic ammonium-oxidizing (anammox) bacteria and the nitrate-sequestering sulphur-oxidizing Thioploca species--in anoxic sediments of the Soledad basin at the Mexican Pacific margin. A mass balance of benthic solute fluxes and the corresponding nitrogen isotope composition of nitrate and ammonium fluxes indicate that anammox bacteria rely on Thioploca species for the supply of metabolic substrates and account for about 57 ± 21 per cent of the total benthic N2 production. We show that Thioploca-anammox symbiosis intensifies benthic fixed nitrogen losses in anoxic sediments, bypassing diffusion-imposed limitations by efficiently coupling the carbon, nitrogen and sulphur cycles.
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