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While there are estimates of the abiotic processes contribution to soil phosphorus (P) availability, less is known about the contribution of biological processes. Two main enzymatic processes involved in soil P cycling are known to alter the oxygen isotopic composition of phosphate (δ18O-P), each in a different way, through the cleavage of the P–O bond: the intracellular P turnover and the organic P hydrolysis. The former induces isotopic equilibration between phosphate and water and is considered the major process affecting soil available P via microbial P release. The latter induces depleted δ18O-P in the phosphate released from the mineralization of organic P. We studied P dynamics in organic horizons of two contrasting soils (low- and high-P availability) from temperate beech forests. We labeled the soil with 18O-enriched water and followed changes in the δ18O-P of different soil P pools in the presence or absence of added leaf litter during 3 months of incubation. δ18O-P values of almost all P pools progressively increased indicating oxygen incorporation from the enriched soil water into phosphate via the above-mentioned enzymatic processes. δ18O-P of available P increased more in the P-rich soil than in the P-poor soil and approached the isotopic equilibrium between phosphate and water, revealing the impact of microbial P release into the available P pool. However, in the P-poor soil, the available P brought the isotopic signature induced by phosphatase enzymes, indicating that it was mostly originated from the hydrolysis of organic P. Therefore, under P-limiting conditions, the isotopic effect of organic P hydrolysis can outweigh the isotopic equilibrium effect. Finally, two independent isotopic approaches with 33P and δ18O-P provided very similar estimates of P exchanged between the available P and other inorganic soil pools. This suggests that δ18O-P can be successfully used to trace P fluxes, provided that the underlying processes do not break the P–O bonds of the phosphate molecule., Frontiers in Environmental Science, 8, ISSN:2296-665X

High atmospheric nitrogen (N) deposition together with climatic changes have been suggested to drive European temperate forests towards phosphorus (P) limitation. In forest ecosystems, trees and microorganisms take up phosphate from the soil solution, which represents a small proportion of total P in soil. To meet P demands, the soil solution must be replenished with P from less labile soil P pools by abiotic (desorption and dissolution) and biotic (solubilization and mineralization) processes. Soil microorganisms contribute to inorganic P solubilization through the release of organic acids and to organic P mineralization through the release of enzymes (e.g. phosphatases). Besides, they synthesize organic P forms. Upon microbial cell death, the microbially synthesized P species return to the soil and can potentially get mineralized or stabilized. Understanding the role of microorganisms in soil P cycling is thus crucial to assess the resilience of forest ecosystems to the increasing imbalance between N and P concentrations. The objective of this thesis was to study the effects of P and N additions on P cycling in the organic (O) soil horizon of temperate beech (Fagus sylvatica L.) forests developed on silicate bedrock. Although not extensively studied, the O horizon is crucial for microbial processes and beech nutrition, particularly under low P availability. Inputs of P and N were hypothesized to affect microbial activity, microbial community composition and the processes microorganisms modulate. Consequently, the proportions of inorganic and organic P pools and forms were expected to change. The effects of P and N inputs were assumed to depend on the initial nutrient status of the soils, which is defined by the underlying parent material. To gain a holistic view, several experimental (field and incubation experiments) and methodological approaches (chemical extractions, spectroscopy, isotopic tracing, enzyme assays, and molecular fingerprinting) were combined. In chapter 1, bacterial (16S rRNA), fungal (ITS), and alkaline (phoD) and acid (acpA) phosphatase harbouring bacterial community responses to changes in soil N and P concentrations in the O horizon were investigated. A field experiment with water-soluble N and P additions was conducted at two beech forest sites with contrasting P stocks (low-P site Lüss (LUE) and high-P site Bad-Brückenau (BBR)). In BBR, microbial community structure changed in response to the increase in resin P induced by the P addition. In LUE, microbial community structure changed in response to decreasing P concentrations in several soil P pools induced by the N addition. Furthermore, the increased importance of strategies to access organic P forms in sites with low P supply from minerals was reflected by a higher relative abundance of some dominant phoD harbouring taxa in LUE than in BBR. In chapter 2, the fate of the 33P-labelled P fertilizer was traced into soil P pools and the impact of enzyme-mediated P cycling processes was determined by the level of incorporation of 18O from 18O-enriched water into phosphate in the field. During a dry summer, a field experiment with water-soluble N and P additions was conducted at a guarded beech forest site in Jülich (JUE). Approximately 40% of P fertilizer was recovered in the studied soil layer, the majority being in inorganic P pools independent of N addition. However, the incorporation of 18O into resin P was mainly stimulated by N addition. In chapter 3, the organic soil horizons from two beech forest sites with contrasting P stocks (low-P site LUE and high-P site Vessertal (VES)) were subjected to four nutrient addition treatments (control without addition, P addition, combined carbon (C) and N addition, combined CNP addition) in an incubation experiment of 103 days. Enzyme-mediated P cycling processes were assessed by studying the oxygen (O) incorporation from 18O-enriched water into phosphate. Phosphorus fluxes into sequentially extracted P pools were traced by labelling the added water-soluble P with 33P. Furthermore, the chemical nature of P in NaOH/EDTA extracts was studied with solution 31P NMR spectroscopy. In the LUE O horizon, half of the added P was recovered in the microbial and organic P pools, while 31P NMR revealed increases in the P classes polyphosphates, phosphonates, and phosphodiesters following inorganic P addition. In contrast, in the VES O horizon, added P was mainly recovered in inorganic P pools. Overall, P and N additions were shown to influence the soil microbial communities and the biological processes they modulate, the P fluxes between soil P pools, and the forms of P present in O horizons of temperate beech forests. On the short-term (days) and under unfavourable environmental conditions for microorganisms, abiotic processes dominated the response to inorganic P addition. In contrast, on a longer-term (months), the P stock, as influenced by the underlying parent material, determined the response to P additions. Abiotic processes dominated in high-P and biotic processes in low-P sites. In the O horizons of low-P sites, microorganisms are strongly interacting with soil organic P, as they mineralize and produce organic P forms. These microbial P cycling processes can be negatively affected by N deposition and extreme environmental conditions (e.g. drought or heat waves). In low-P sites, N addition can induce decreases in soil P pool concentrations, which affects microbial communities (Chapter 1), and can reduce microbial organic P synthesis (Chapter 3). Dry conditions can reduce the influence of biotic processes on P fluxes (Chapter 2). High N deposition and extreme environmental conditions thus represent a greater threat to low-P O horizons with high competition for P than to high-P O horizons.