Maria Mooshammer

Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea

Soil emissions are largely responsible for the increase of the potent greenhouse gas nitrous oxide (N2O) in the atmosphere and are generally attributed to the activity of nitrifying and denitrifying bacteria. However, the contribution of the recently discovered ammonia-oxidizing archaea (AOA) to N2O production from soil is unclear as is the mechanism by which they produce it. Here we investigate the potential of Nitrososphaera viennensis, the first pure culture of AOA from soil, to produce N2O and compare its activity with that of a marine AOA and an ammonia-oxidizing bacterium (AOB) from soil. N. viennensis produced N2O at a maximum yield of 0.09% N2O per molecule of nitrite under oxic growth conditions. N2O production rates of 4.6±0.6 amol N2O cell−1 h−1 and nitrification rates of 2.6±0.5 fmol NO2− cell−1 h−1 were in the same range as those of the AOB Nitrosospira multiformis and the marine AOA Nitrosopumilus maritimus grown under comparable conditions. In contrast to AOB, however, N2O production of the two archaeal strains did not increase when the oxygen concentration was reduced, suggesting that they are not capable of denitrification. In 15N-labeling experiments we provide evidence that both ammonium and nitrite contribute equally via hybrid N2O formation to the N2O produced by N. viennensis under all conditions tested. Our results suggest that archaea may contribute to N2O production in terrestrial ecosystems, however, they are not capable of nitrifier-denitrification and thus do not produce increasing amounts of the greenhouse gas when oxygen becomes limiting.

Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources

Terrestrial microbial decomposer communities thrive on a wide range of organic matter types that rarely ever meet their elemental demands. In this review we synthesize the current state-of-the-art of microbial adaptations to resource stoichiometry, in order to gain a deeper understanding of the interactions between heterotrophic microbial communities and their chemical environment. The stoichiometric imbalance between microbial communities and their organic substrates generally decreases from wood to leaf litter and further to topsoil and subsoil organic matter. Microbial communities can respond to these imbalances in four ways: first, they adapt their biomass composition toward their resource in a non-homeostatic behavior. Such changes are, however, only moderate, and occur mainly because of changes in microbial community structure and less so due to cellular storage of elements in excess. Second, microbial communities can mobilize resources that meet their elemental demand by producing specific extracellular enzymes, which, in turn, is restricted by the C and N requirement for enzyme production itself. Third, microbes can regulate their element use efficiencies (ratio of element invested in growth over total element uptake), such that they release elements in excess depending on their demand (e.g., respiration and N mineralization). Fourth, diazotrophic bacteria and saprotrophic fungi may trigger the input of external N and P to decomposer communities. Theoretical considerations show that adjustments in element use efficiencies may be the most important mechanism by which microbes regulate their biomass stoichiometry. This review summarizes different views on how microbes cope with imbalanced supply of C, N and P, thereby providing a framework for integrating and linking microbial adaptation to resource imbalances to ecosystem scale fluxes across scales and ecosystems.

The application of ecological stoichiometry to plant–microbial–soil organic matter transformations

Elemental stoichiometry constitutes an inherent link between biogeochemistry and the structure and processes within food webs, and thus is at the core of ecosystem functioning. Stoichiometry allows for spanning different levels of biological organization, from cellular metabolism to ecosystem structure and nutrient cycling, and is therefore particularly useful for establishing links between different ecosystem compartments. We review elemental carbon : nitrogen : phosphorus (C:N:P) ratios in terrestrial ecosystems (from vegetation, leaf litter, woody debris, and dead roots, to soil microbes and organic matter). While the stoichiometry of the plant, litter, and soil compartments of ecosystems is well understood, heterotrophic microbial communities, which dominate the soil food web and drive nutrient cycling, have received increasing interest in recent years. This review highlights the effects of resource stoichiometry on soil microorganisms and decomposition, specifically on the structure and function of h...

Stoichiometric controls of nitrogen and phosphorus cycling in decomposing beech leaf litter

Resource stoichiometry (C:N:P) is an important determinant of litter decomposition. However, the effect of elemental stoichiometry on the gross rates of microbial N and P cycling processes during litter decomposition is unknown. In a mesocosm experiment, beech (Fagus sylvatica L.) litter with natural differences in elemental stoichiometry (C:N:P) was incubated under constant environmental conditions. After three and six months, we measured various aspects of nitrogen and phosphorus cycling. We found that gross protein depolymerization, N mineralization (ammonification), and nitrification rates were negatively related to litter C:N. Rates of P mineralization were negatively correlated with litter C:P. The negative correlations with litter C:N were stronger for inorganic N cycling processes than for gross protein depolymerization, indicating that the effect of resource stoichiometry on intracellular processes was stronger than on processes catalyzed by extracellular enzymes. Consistent with this, extracellular protein depolymerization was mainly limited by substrate availability and less so by the amount of protease. Strong positive correlations between the interconnected N and P pools and the respective production and consumption processes pointed to feed-forward control of microbial litter N and P cycling. A negative relationship between litter C:N and phosphatase activity (and between litter C:P and protease activity) demonstrated that microbes tended to allocate carbon and nutrients in ample supply into the production of extracellular enzymes to mine for the nutrient that is more limiting. Overall, the study demonstrated a strong effect of litter stoichiometry (C:N:P) on gross processes of microbial N and P cycling in decomposing litter; mineralization of N and P were tightly coupled to assist in maintaining cellular homeostasis of litter microbial communities.

Plant community type and small‐scale disturbances, but not altitude, influence the invasibility in subarctic ecosystems

Little of our knowledge about invasibility comes from arctic and alpine ecosystems, despite increasing plant migration and invasion in those regions. Here, we examine how community type, altitude, and small-scale disturbances affect invasibility in a subarctic ecosystem. Over a period of 4 yr, we studied seedling emergence and establishment in 17 species sown in gaps or undisturbed vegetation in four subarctic community types (Salix scrub, meadow, rich heath, poor heath) along an elevation gradient. Invasibility was lowest in rich heath and highest in Salix scrub. Small disturbances significantly increased the invasibility in most communities, thereby showing the importance of biotic resistance to invasion in subarctic regions. Unexpectedly, invasibility did not decrease with increasing elevation, and it was also not related to summer temperature. Our data suggest that biotic resistance might be more important than abiotic stress for invasibility in subarctic tundra and that low temperatures do not necessarily limit seedling establishment at high altitudes. High elevations are therefore potentially more vulnerable to invasion than was originally thought. Changes in community composition as a result of species migration or invasion are most likely to occur in Salix scrub and meadow, whereas Empetrum-dominated rich heath will largely remain unchanged.

Microbial nitrogen dynamics in organic and mineral soil horizons along a latitudinal transect in western Siberia.

Soil N availability is constrained by the breakdown of N-containing polymers such as proteins to oligopeptides and amino acids that can be taken up by plants and microorganisms. Excess N is released from microbial cells as ammonium (N mineralization), which in turn can serve as substrate for nitrification. According to stoichiometric theory, N mineralization and nitrification are expected to increase in relation to protein depolymerization with decreasing N limitation, and thus from higher to lower latitudes and from topsoils to subsoils. To test these hypotheses, we compared gross rates of protein depolymerization, N mineralization and nitrification (determined using 15N pool dilution assays) in organic topsoil, mineral topsoil, and mineral subsoil of seven ecosystems along a latitudinal transect in western Siberia, from tundra (67°N) to steppe (54°N). The investigated ecosystems differed strongly in N transformation rates, with highest protein depolymerization and N mineralization rates in middle and southern taiga. All N transformation rates decreased with soil depth following the decrease in organic matter content. Related to protein depolymerization, N mineralization and nitrification were significantly higher in mineral than in organic horizons, supporting a decrease in microbial N limitation with depth. In contrast, we did not find indications for a decrease in microbial N limitation from arctic to temperate ecosystems along the transect. Our findings thus challenge the perception of ubiquitous N limitation at high latitudes, but suggest a transition from N to C limitation of microorganisms with soil depth, even in high-latitude systems such as tundra and boreal forest. Key Points We compared soil N dynamics of seven ecosystems along a latitudinal transect Shifts in N dynamics suggest a decrease in microbial N limitation with depth We found no decrease in microbial N limitation from arctic to temperate zones

Optimal metabolic regulation along resource stoichiometry gradients

Most heterotrophic organisms feed on substrates that are poor in nutrients compared to their demand, leading to elemental imbalances that may constrain their growth and function. Flexible carbon (C)-use efficiency (CUE, C used for growth over C taken up) can represent a strategy to reduce elemental imbalances. Here, we argue that metabolic regulation has evolved to maximise the organism growth rate along gradients of nutrient availability and translated this assumption into an optimality model that links CUE to substrate and organism stoichiometry. The optimal CUE is predicted to decrease with increasing substrate C-to-nutrient ratio, and increase with nutrient amendment. These predictions are generally confirmed by empirical evidence from a new database of c. 2200 CUE estimates, lending support to the hypothesis that CUE is optimised across levels of organisation (microorganisms and animals), in aquatic and terrestrial systems, and when considering nitrogen or phosphorus as limiting nutrients.

Metabolism of mineral-sorbed organic matter and microbial lifestyles in fluvial ecosystems

In fluvial ecosystems mineral erosion, carbon (C), and nitrogen (N) fluxes are linked via organomineral complexation, where dissolved organic molecules bind to mineral surfaces. Biofilms and suspended aggregates represent major aquatic microbial lifestyles whose relative importance changes predictably through fluvial networks. We tested how organomineral sorption affects aquatic microbial metabolism, using organomineral particles containing a mix of 13C, 15N-labeled amino acids. We traced 13C and 15N retention within biofilm and suspended aggregate biomass and its mineralization. Organomineral complexation restricted C and N retention within biofilms and aggregates and also their mineralization. This reduced the efficiency with which biofilms mineralize C and N by 30% and 6%. By contrast, organominerals reduced the C and N mineralization efficiency of suspended aggregates by 41% and 93%. Our findings show how organomineral complexation affects microbial C:N stoichiometry, potentially altering the biogeochemical fate of C and N within fluvial ecosystems.

Decoupling of microbial carbon, nitrogen, and phosphorus cycling in response to extreme temperature events

Analysis of disturbance effects on multiple microbial processes elucidates response of biogeochemical cycling to climate extremes. Predicted changes in the intensity and frequency of climate extremes urge a better mechanistic understanding of the stress response of microbially mediated carbon (C) and nutrient cycling processes. We analyzed the resistance and resilience of microbial C, nitrogen (N), and phosphorus (P) cycling processes and microbial community composition in decomposing plant litter to transient, but severe, temperature disturbances, namely, freeze-thaw and heat. Disturbances led temporarily to a more rapid cycling of C and N but caused a down-regulation of P cycling. In contrast to the fast recovery of the initially stimulated C and N processes, we found a slow recovery of P mineralization rates, which was not accompanied by significant changes in community composition. The functional and structural responses to the two distinct temperature disturbances were markedly similar, suggesting that direct negative physical effects and costs associated with the stress response were comparable. Moreover, the stress response of extracellular enzyme activities, but not that of intracellular microbial processes (for example, respiration or N mineralization), was dependent on the nutrient content of the resource through its effect on microbial physiology and community composition. Our laboratory study provides novel insights into the mechanisms of microbial functional stress responses that can serve as a basis for field studies and, in particular, illustrates the need for a closer integration of microbial C-N-P interactions into climate extremes research.

Full 15 N tracer accounting to revisit major assumptions of 15 N isotope pool dilution approaches for gross nitrogen mineralization

The 15N isotope pool dilution (IPD) technique is the only available method for measuring gross ammonium (NH4+) production and consumption rates. Rapid consumption of the added 15N-NH4+ tracer is commonly observed, but the processes responsible for this consumption are not well understood. The primary objectives of this study were to determine the relative roles of biotic and abiotic processes in 15N-NH4+ sconsumption and to investigate the validity of one of the main assumptions of IPD experiments, i.e., that no reflux of the consumed 15N tracer occurs during the course of the experiments. We added a 15N-NH4+ tracer to live and sterile (autoclaved) soil using mineral topsoil from a beech forest and a grassland in Austria that differed in NH4+ concentrations and NH4+ consumption kinetics. We quantified both biotic tracer consumption (i.e. changes in the concentrations and 15N enrichments of NH4+, dissolved organic N (DON), NO3− and the microbial N pool) and abiotic tracer consumption (i.e., fixation by clay and/or humic substances). We achieved full recovery of the 15N tracer in both soils over the course of the 48 h incubation. For the forest soil, we found no rapid consumption of the 15N tracer, and the majority of tracer (78%) remained unconsumed at the end of the incubation period. In contrast, the grassland soil showed rapid 15N-NH4+ consumption immediately after tracer addition, which was largely due to both abiotic fixation (24%) and biotic processes, largely uptake by soil microbes (10%) and nitrification (13%). We found no evidence for reflux of 15N-NH4+ over the 48 h incubation period in either soil. Our study therefore shows that 15N tracer reflux during IPD experiments is negligible for incubation times of up to 48 h, even when rapid NH4+ consumption occurs. Such experiments are thus robust to the assumption that immobilized labeled N is not re–mobilized during the experimental period and does not impact calculations of gross N mineralization.