Benthic foraminifera are unicellular eukaryotes found abundantly in many types of marine sediments. Many species survive and possibly reproduce in anoxic habitats, but sustainable anaerobic metabolism has not been previously described. Here we demonstrate that the foraminifer Globobulimina pseudospinescens accumulates intracellular nitrate stores and that these can be respired to dinitrogen gas. The amounts of nitrate detected are estimated to be sufficient to support respiration for over a month. In a Swedish fjord sediment where G. pseudospinescens is the dominant foraminifer, the intracellular nitrate pool in this species accounted for 20% of the large, cell-bound, nitrate pool present in an oxygen-free zone. Similarly high nitrate concentrations were also detected in foraminifera Nonionella cf. stella and a Stainforthia species, the two dominant benthic taxa occurring within the oxygen minimum zone of the continental shelf off Chile. Given the high abundance of foraminifera in anoxic marine environments, these new findings suggest that foraminifera may play an important role in global nitrogen cycling and indicate that our understanding of the complexity of the marine nitrogen cycle is far from complete.
Benthic foraminifers inhabit a wide range of aquatic environments including open marine, brackish, and freshwater environments. Here we show that several different and diverse foraminiferal groups (miliolids, rotaliids, textulariids) and Gromia , another taxon also belonging to Rhizaria, accumulate and respire nitrates through denitrification. The widespread occurrence among distantly related organisms suggests an ancient origin of the trait. The diverse metabolic capacity of these organisms, which enables them to respire with oxygen and nitrate and to sustain respiratory activity even when electron acceptors are absent from the environment, may be one of the reasons for their successful colonization of diverse marine sediment environments. The contribution of eukaryotes to the removal of fixed nitrogen by respiration may equal the importance of bacterial denitrification in ocean sediments.
A meta-analysis was conducted on 136 data sets of denitrification rates (DR) recorded both during the period of highest water temperature and monthly in five types of aquatic ecosystems: oceans, coastal environments, estuaries, lakes and rivers. There was a gradual increase of DR from the ocean to rivers and lakes at both scales, with the rivers showing the highest DR variability. Denitrification peaked during summertime and showed highest seasonal variability in lakes and rivers. High concentrations of nitrate and interstitially-dissolved organic carbon as well as low oxygen concentration in the overlying water enhanced DR both during summer and at a seasonal scale whereas total phosphorus did at the seasonal scale only. There was a positive linear relationship between overlying nitrate and DR over the range of 1-970 lmol NO 3 (r 2 = 0.86, P = 0.001). DR in lakes and rivers might reach values doubling those in the more denitrifying terrestrial ecosystems (e.g. agrosystems). Discrepancies in DR and its controlling factors between site-specific studies and this meta-analysis may arise from environmental variability at two, often confounded, scales of observation: the habitat and the ecosystem level. Future studies on denitrification in aquatic environments should address the topic of spatial heterogeneity more thoroughly.
NO 3À isotope labelling experiments were performed to investigate foraminiferal nitrate uptake strategies and the role of pseudopodial networks in nitrate uptake. Globobulimina turgida were placed below the nitrate penetration depth in homogenized sediment cores incubated in artificial seawater containing 15 NO 3 À. A nylon net prevented the vertical migration of foraminifera to strata containing nitrate and oxygen, but allowed potential access to such strata by extension of pseudopods. No 15 NO 3 À was found in G. turgida in these cores, suggesting that foraminifera cannot extend their pseudopods for nitrate uptake through several millimetres of sediment, but must physically migrate upwards closer to nitratecontaining strata. However, foraminiferal migration patterns in control cores with no nylon net were erratic, suggesting that individuals move in random orientations until they find favourable conditions (i.e. free nitrate or oxygen). A second experiment showed that foraminifera actively collect nitrate both in the presence and in the absence of oxygen, although uptake was initiated faster if oxygen was absent from the environment. However, no systematic influence of the size of the intracellular nitrate pool on nitrate uptake was observed, as specimens containing a large range of intracellular nitrate (636-19 992 pmol per cell) were measured to take up 15 NO 3 À at comparable rates.
In a laboratory experiment, we examined the prolonged survival and behaviour of the benthic foraminiferan Globobulimina turgida under 3 simulated natural conditions: oxygenated with added nitrate, anoxic with added nitrate, and anoxic. The survival rates, adenosine triphosphate (ATP) reserve and intracellular nitrate pool of G. turgida were measured periodically under these conditions. Furthermore, to evaluate the efficiency and energy yield of the respiration system, denitrification rates of individual specimens were quantified using the acetylene inhibition and N 2 O microsensor technique at the start of the experiment. Our results demonstrate that the long-term (56 d) survival rate (64%) and ATP concentrations of G. turgida were not significantly different in oxygenated and anoxic, nitrate-containing conditions (Mann-Whitney test, p > 0.05). Thus, G. turgida can survive prolonged anoxia (3 mo) as long as nitrate is available to sustain its respiration. However, it remains unsure whether growth or reproduction can take place under anoxia. Short-term (21 to 35 d) survival rates were lower in nitrate-free, anoxic conditions (22% recovered alive compared to 62 to 82% in nitrate-oxic or nitrate-anoxic conditions), but foraminifera were observed to survive up to 56 d if respiring from their intra-cellular nitrate pool only. The foraminiferal nitrate pool appears very dynamic, as wide ranges of concentrations were measured in living specimens (0 to 463 mM ind.-1 ). We postulate that the scatter in the nitrate pool measurements highlights the ability of the foraminifera to actively collect and respire on nitrate, depending on individuals' history of exposure to oxygen and nitrate.
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