Carbohydrate depletion in roots impedes phosphorus nutrition in young forest trees.

Nutrient imbalances cause the deterioration of tree health in European forests, but the underlying physiological mechanisms are unknown. Here, we investigated the consequences of decreasing root carbohydrate reserves for phosphorus (P) mobilisation and uptake by forest trees. In P-rich and P-poor beech (Fagus sylvatica) forests, naturally grown, young trees were girdled and used to determine root, ectomycorrhizal and microbial activities related to P mobilisation in the organic layer and mineral topsoil in comparison with those in nongirdled trees. After girdling, root carbohydrate reserves decreased. Root phosphoenolpyruvate carboxylase activities linking carbon and P metabolism increased. Root and ectomycorrhizal phosphatase activities and the abundances of bacterial genes catalysing major steps in P turnover increased, but soil enzymes involved in P mobilisation were unaffected. The physiological responses to girdling were stronger in P-poor than in P-rich forests. P uptake was decreased after girdling. The soluble and total P concentrations in roots were stable, but fine root biomass declined after girdling. Our results support that carbohydrate depletion results in reduced P uptake, enhanced internal P remobilisation and root biomass trade-off to compensate for the P shortage. As reductions in root biomass render trees more susceptible to drought, our results link tree deterioration with disturbances in the P supply as a consequence of decreased belowground carbohydrate allocation.

Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems.

Phosphorus (P) is an important macronutrient for all biota on earth but similarly a finite resource. Microorganisms play on both sides of the fence as they effectively mineralize organic and solubilize precipitated forms of soil phosphorus but conversely also take up and immobilize P. Therefore, we analysed the role of microbes in two beech forest soils with high and low P content by direct sequencing of metagenomic deoxyribonucleic acid. For inorganic P solubilization, a significantly higher microbial potential was detected in the P-rich soil. This trait especially referred to Candidatus Solibacter usiatus, likewise one of the dominating species in the data sets. A higher microbial potential for efficient phosphate uptake systems (pstSCAB) was detected in the P-depleted soil. Genes involved in P starvation response regulation (phoB, phoR) were prevalent in both soils. This underlines the importance of effective phosphate (Pho) regulon control for microorganisms to use alternative P sources during phosphate limitation. Predicted genes were primarily harboured by Rhizobiales, Actinomycetales and Acidobacteriales.

Soil phosphorus status and P nutrition strategies of European beech forests on carbonate compared to silicate parent material.

Sustainable forest management requires understanding of ecosystem phosphorus (P) cycling. Lang et al. (2017) [Biogeochemistry, https://doi.org/10.1007/s10533-017-0375-0] introduced the concept of P-acquiring vs. P-recycling nutrition strategies for European beech (Fagus sylvatica L.) forests on silicate parent material, and demonstrated a change from P-acquiring to P-recycling nutrition from P-rich to P-poor sites. The present study extends this silicate rock-based assessment to forest sites with soils formed from carbonate bedrock. For all sites, it presents a large set of general soil and bedrock chemistry data. It thoroughly describes the soil P status and generates a comprehensive concept on forest ecosystem P nutrition covering the majority of Central European forest soils. For this purpose, an Ecosystem P Nutrition Index (ENI P ) was developed, which enabled the comparison of forest P nutrition strategies at the carbonate sites in our study among each other and also with those of the silicate sites investigated by Lang et al. (2017). The P status of forest soils on carbonate substrates was characterized by low soil P stocks and a large fraction of organic Ca-bound P (probably largely Ca phytate) during early stages of pedogenesis. Soil P stocks, particularly those in the mineral soil and of inorganic P forms, including Al- and Fe-bound P, became more abundant with progressing pedogenesis and accumulation of carbonate rock dissolution residue. Phosphorus-rich impure, silicate-enriched carbonate bedrock promoted the accumulation of dissolution residue and supported larger soil P stocks, mainly bound to Fe and Al minerals. In carbonate-derived soils, only low P amounts were bioavailable during early stages of pedogenesis, and, similar to P-poor silicate sites, P nutrition of beech forests depended on tight (re)cycling of P bound in forest floor soil organic matter (SOM). In contrast to P-poor silicate sites, where the ecosystem P nutrition strategy is direct biotic recycling of SOM-bound organic P, recycling during early stages of pedogenesis on carbonate substrates also involves the dissolution of stable Ca-Porg precipitates formed from phosphate released during SOM decomposition. In contrast to silicate sites, progressing pedogenesis and accumulation of P-enriched carbonate bedrock dissolution residue at the carbonate sites promote again P-acquiring mechanisms for ecosystem P nutrition. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10533-021-00884-7.

Novel oligonucleotide primers reveal a high diversity of microbes which drive phosphorous turnover in soil.

Phosphorus (P) is of central importance for cellular life but likewise a limiting macronutrient in numerous environments. Certainly microorganisms have proven their ability to increase the phosphorus bioavailability by mineralization of organic-P and solubilization of inorganic-P. On the other hand they efficiently take up P and compete with other biota for phosphorus. However the actual microbial community that is associated to the turnover of this crucial macronutrient in different ecosystems remains largely anonymous especially taking effects of seasonality and spatial heterogeneity into account. In this study seven oligonucleotide primers are presented which target genes coding for microbial acid and alkaline phosphatases (phoN, phoD), phytases (appA), phosphonatases (phnX) as well as the quinoprotein glucose dehydrogenase (gcd) and different P transporters (pitA, pstS). Illumina amplicon sequencing of soil genomic DNA underlined the high rate of primer specificity towards the respective target gene which usually ranged between 98% and 100% (phoN: 87%). As expected the primers amplified genes from a broad diversity of distinct microorganisms. Using DNA from a beech dominated forest soil, the highest microbial diversity was detected for the alkaline phosphatase (phoD) gene which was amplified from 15 distinct phyla respectively 81 families. Noteworthy the primers also allowed amplification of phoD from 6 fungal orders. The genes coding for acid phosphatase (phoN) and the quinoprotein glucose dehydrogenase (gcd) were amplified from 20 respectively 17 different microbial orders. In comparison the phytase and phosphonatase (appA, phnX) primers covered 13 bacterial orders from 2 different phyla respectively. Although the amplified microbial diversity was apparently limited both primers reliably detected all orders that contributed to the P turnover in the investigated soil as revealed by a previous metagenomic approach. Genes that code for microbial P transporter (pitA, pstS) were amplified from 13 respectively 9 distinct microbial orders. Accordingly the introduced primers represent a valuable tool for further analysis of the microbial community involved in the turnover of phosphorus in soils but most likely also in other environments.

An inter-laboratory comparison of gaseous and liquid fumigation based methods for measuring microbial phosphorus (Pmic) in forest soils with differing P stocks.

In an inter-laboratory trial, gaseous ("CFE") and liquid fumigation ("Resin") based methods for measuring microbial phosphorus (Pmic) were compared, based on the analysis of soil samples from five forests, which differ in their P stocks. Both methods reliably detected the same Pmic gradient in the different soils. However, when the individual recovery rates of spiked P were taken into account, the "CFE" based methods consistently generated higher Pmic values (factor 2) compared to the "Resin" based approaches.