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Faculty for Biology, Chemistry and Earth Sciences

Department Soil Ecology - Prof. Dr. Eva Lehndorff

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PhD Thesis

Element cycling in grassland soils as driven by stoichiometric homeostasis of microorganisms.

Meike Widdig (12/2016-11/2021)

Support: Marie Spohn


An unprecedented increase in nitrogen (N) emissions since the 1970s has changed soils N-to- phosphorus (P) stoichiometry, i.e. the relation of N and P in soil. Yet, the consequences of increased nutrient supply on microbial communities and soil element cycling driven by microorganisms are poorly understood. Relatively constrained element ratios in the microbial biomass have been found, indicating stoichiometric homeostasis of microbial biomass. Thus, independent of their surroundings, microorganisms keep a relatively constant biomass carbon (C):N:P ratio, whereas the resources they feed on can have much larger and highly variable element ratios. The concept of Ecological Stoichiometry explains ecological processes based on their elemental ratios and thus by acknowledging chemical constraints on organismal functioning. Yet, it is unclear if Ecological Stoichiometry can be used as a framework predicting element cycling in terrestrial ecosystems. A main research question of this thesis was if microorganisms largely drive C, N, and P cycling in grassland soils by maintaining their biomass stoichiometry. To do the latter, microorganisms are thought to adjust processes of element partitioning and turnover, as well as of element acquisition. Novel isotopic methods enabled us to study microbial element partitioning and turnover, two processes that largely determine element cycling. To understand element cycling in grasslands on a global scale, we studied six experimental sites on three continents. Seven to nine years of N, P, and NP additions allowed us to study the consequences of changing element inputs on soil microbial element partitioning, turnover, and acquisition. We used novel isotopic methods based on ¹⁸O and ³³P labelling of the microbial DNA to study carbon use efficiency (CUE) and element turnover times in the microbial biomass. We determined microbial biomass C and N with chloroform-fumigation, net C and N mineralization in incubation experiments, extracellular enzyme activities with fluorogenic substrates, and non-symbiotic N₂ fixation in a ¹⁵N labelled atmosphere. Further, we used physiological assays to screen for P-solubilizing bacteria (PSB) and we analyzed the PSB and the microbial community via Sanger and Illumina Sequencing, respectively. After years of nutrient addition, ratios of available soil elements strongly changed, whereas microbial biomass stoichiometry was unaffected confirming the concept of stoichiometric homeostasis. Microbial C partitioning, the ratio between C allocated to growth and C taken up, called soil microbial CUE, correlated with substrate stoichiometry. Microorganisms respired less when substrate stoichiometry was closer to their own biomass stoichiometry, whereas they respired more when thriving on substrate with a more unfavorable stoichiometry. Besides element partitioning, microorganisms adjusted turnover times of elements in their biomass. For the first time, we showed that with decreasing P availability, the mean residence time of P in the microbial biomass increased likely because microorganisms recycled P more efficiently internally. Besides C partitioning and P turnover, microorganisms adjusted processes of element acquisition to their stoichiometric demands. Non-symbiotic N₂ fixation was correlated with soil N:P ratios showing that the energy-consuming process of N₂ fixation depended on sufficient P to enable ATP production and at the same time on low N availabilities. Microbial release of N, net N mineralization, was highly dependent on substrate stoichiometry in the way that microorganisms released more N, when N compared to C availability was high and vice versa. However, the activity of leucine-aminopeptidase, a N-acquiring enzyme, was not related to substrate stoichiometry. Further, the relative abundance of PSB was related to soil C:P ratios indicating that the production of organic acids, that solubilize P, needs sufficient C sources. Organic P can be mineralized through phosphatases, extracellular enzymes. Phosphatase activity increased with rising N availability indicating that (i) microbial P demand increased to maintain biomass stoichiometry and that (ii) more N enabled the production of enzymes. Further, element availabilities were the main drivers of element cycling as opposed to microbial community change at one site in the USA confirming the importance of element availabilities on element cycling in grasslands. In conclusion, Ecological Stoichiometry has proven to be a promising tool for explaining and predicting various element cycling rates in grasslands. However, it needs to be considered that besides element ratios climatic variables, soil pH, and soil texture impacted element cycling rates. Further, not all processes, such as leucine-aminopeptidase activity, were driven by microbial homeostasis. Nevertheless, based on stoichiometric homeostasis of soil microorganisms, many element cycling rates can be understood and predicted in more detail. Thus, Ecological Stoichiometry should be considered as a key concept in terrestrial ecology.

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