Temporal variations of phosphorus uptake by soil microbial biomass and young beech trees in two forest soils with contrasting phosphorus stocks
Introduction
Despite the importance of phosphorus (P) for plant nutrition, little is known about the temporal patterns of plant P uptake in forest ecosystems and about the factors that control them (Vance et al., 2003, Plassard and Dell, 2010). During the last decades, foliar P concentrations of several tree species in temperate forests have decreased, and the reasons for this decrease are not yet known (Flückiger and Braun, 1998, Duquesnay et al., 2000, Ilg et al., 2009, Braun et al., 2010, Crowley et al., 2012, Jonard et al., 2015, Talkner et al., 2015). This calls for a better understanding of P dynamics in the interplay of soil, ectomycorrhizal fungi (EMF), soil microbial biomass (SMB), and plant and microbial activities in temperate forests.
P availability in soil is largely affected by sorption (Hinsinger, 2001, Giesler et al., 2002). Since phosphate is rapidly sorbed to the soil matrix, only a small proportion of the total soil P is plant available. Thus, plants, bacteria and especially EMF have developed several mechanisms to solubilize bound inorganic P by releasing organic acid anions, protons and siderophores (Jones and Oburger, 2011, Jansa et al., 2011, Smits et al., 2012). Furthermore, they can mineralize organic P by releasing extracellular phosphatases, which renders P plant available (Plassard and Dell, 2010, Nannipieri et al., 2011). Microbial organic phosphorus mineralization in the vicinity of the root can increase the plant available inorganic P concentration (Richardson et al., 2009, Spohn et al., 2013). Besides mobilizing P, EMF can be very efficient in P uptake from soil because their hyphae reach micropores that are not accessible to roots and have a very high surface area-to-volume ratio (Jansa et al., 2011).
Only few studies explored P uptake kinetics of ectomycorrhizal-forming tree species (Van Tichelen and Colpaert, 2000, Brandtberg et al., 2004, Jonard et al., 2009, Desai et al., 2014, Kavka and Polle, 2016). Tracer studies with 33P showed that P uptake systems of non-mycorrhizal roots are limited because their Michaelis-Menten constants (Km) are higher than typical concentrations of free Pi in the soil solution (Van Tichelen and Colpaert, 2000, Desai et al., 2014, Kavka and Polle, 2016). In mycorrhizal trees, the Km is strongly decreased and the uptake rate drastically enhanced (Van Tichelen and Colpaert, 2000, Desai et al., 2014), which underpins the relevance of EMF for plant P uptake. It is not known yet, whether high plant P uptake is associated with a specific EMF community or whether there is a functional redundancy in EMF communities with respect to P mobilization. Moreover, since previous experiments (Van Tichelen and Colpaert, 2000) were conducted in hydroponic solutions in the absence of soil bacteria and saprotrophic fungi, which may strongly affect tree nutrient uptake, the environmental factors that influence P acquisition of EMF and their host trees are still unknown.
Microbial biomass P can represent a substantial fraction of the total soil P. In temperate coniferous and broadleaf forests it amounts on average to 4.3 and 8.6% of the total P in the mineral soil, respectively (Xu et al., 2013). In the organic layer of beech forests, about 22–47% of the total P is sequestered in the microbial biomass (Zederer et al., 2017). Especially in relatively nutrient poor temperate forests with the humus form moder, a large proportion of the total soil P is stored in the SMB (Zederer et al., 2017).
While there are only few studies that explored P uptake kinetics of trees and microorganisms using 33P, uptake kinetics have been studied more intensively for nitrogen (N) using 15N. In many studies, in which N uptake by trees and SMB was compared, it was found that initially the SMB took up a significantly larger percentage of the added 15N than the tree. This was documented for Acer saccharum in northern hardwood forests (Zogg et al., 2000), for Quercus douglasii in California (Cheng and Bledsoe, 2004), for birch forests in subarctic Sweden (Grogan and Jonasson, 2003), for Fraxinus excelsior in France (Bloor et al., 2009), and for Fagus sylvatica in Germany (Pena et al., 2013, Leberecht et al., 2015, Dannenmann et al., 2016). 15N immobilized in the SMB was only very slowly released during the following months (Zogg et al., 2000, Grogan and Jonasson, 2003).
In ecosystems with pronounced seasonality, such as temperate and alpine ecosystems, plant N uptake and microbial N uptake are often anticyclical in the way that plants take up N mostly during the growing season, while microbial N uptake is highest in autumn, stimulated by high inputs of leaf litter during this time of the year (Jaeger et al., 1999, Lipson et al., 1999, Kaiser et al., 2011). At the end of winter, microbial N decreases again due to thawing-and-freezing events that induce microbial cell lysis (Jaeger et al., 1999, Lipson et al., 1999, Kaiser et al., 2011). It is not known yet, whether such dynamics also occur in temperate forest soils with respect to P uptake.
The objective of this study was to determine temporal variations of P uptake by SMB and by young beech trees (Fagus sylvatica) along with the root-associated EMF assemblage, potential acid phosphatase activity (APA) and abundance of the bacterial acid phosphatase (phoN) genes in two forests differing in total P stocks. For this purpose, young beech trees were extracted with intact soil cores from two forest sites that differ in total soil P stocks and P availability (Zavišić et al., 2016), and were exposed to ambient conditions in a common garden study. We hypothesized, first, that uptake of P by beech trees is higher in summer, when the trees are photosynthetically more active than in autumn (Yang et al., 2016), while P uptake by the SMB is highest in autumn due to inputs of plant detritus during this time of the year. Second, we hypothesized that a larger proportion of P is taken up by the SMB in the P-poor forest compared to the P-rich forest throughout the year. Third, we hypothesized that P uptake by F. sylvatica is independent of specific EMF species due to a high diversity and functional redundancy of EMF species.
Section snippets
Study site
Soils and juvenile trees were collected at two sites with contrasting soil P availability (Table 1). The site Bad Brueckenau (BBR) that has a high soil P availability is located in the Rhoen Mountains, close to the city of Fulda, Germany (N 50° 21.38′, E 9° 55.71′) at 825 m above sea-level. The mean annual rainfall is 1031 mm and the mean annual temperature is 5.8 °C. The soil is a Dystric Skeletic Cambisol derived from basalt, and the prevailing tree species is European beech (Fagus sylvatica
EMF, SMB and labile P
The number of root tips colonized by EMF was lower in the mesocosms from the P-poor site LUE than in the mesocosms from the P-rich site BBR throughout the year (p < 0.001; Fig. 1a). The community composition of EMF taxa showed seasonal fluctuations indicated by the separation along coordinate 1 of the NMDS (Fig. 2). The communities in spring and early summer formed one cluster, while a second clustered was formed by the communities in late summer, autumn, and winter (Fig. 2, Additional online
Methodological considerations
This is the first study to show that P uptake rates of a young tree, and of the SMB differ seasonally, and between contrasting forest sites. Since our study was conducted in a common garden, effects of low water availability were avoided, which are known to impact nutrient uptake under field conditions (Bimüller et al., 2014, Dannenmann et al., 2016, Leberecht et al., 2016).
We calculated total P uptake rates based on the 33P uptake and the specific 33P activity of the labile P pool, following
Author contributions
AP designed the experiments, analyzed data, wrote and commented on the manuscript. AZ conducted field work, analyzed samples, analyzed data, wrote and commented on the manuscript. MS analyzed samples, conducted data analysis and wrote the manuscript. PN, SM and EK analyzed APA and commented on the manuscript. SS, MSch and FB analyzed qPCR data and commented on the manuscript. All authors approved the final version of the manuscript.
Acknowledgements
We are grateful to the excellent technical assistance by M. Franke-Klein and the members of the Laboratory for Radio-Isotopes, B. Kopka, T. Klein and G. Lehmann. Financial support was provided by the Deutsche Forschungsgemeinschaft (DFG) to the Collaborative Research Program (Ecosystem Nutrition, SPP1685) by grants to AP (PO362/22-1, 22-2), EK (KA1590/12-1, 12-2), MS (SP1389/4-1, 4-2), and SS (SCHU 2907/3-1, 3-2).
References (79)
- et al.
Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model
Soil Biology and Biochemistry
(2010) - et al.
Novel oligonucleotide primers reveal a high diversity of microbes which drive phosphorous turnover in soil
Journal of Microbiological Methods
(2016) - et al.
Prolonged summer droughts retard soil N processing and stabilization in organo-mineral fractions
Soil Biology and Biochemistry
(2014) - et al.
CO2 and inorganic N supply modify competition for N between co-occurring grass plants, tree seedlings and soil microorganisms
Soil Biology and Biochemistry
(2009) - et al.
Distributions of the capacity to take up nutrients by Betula spp. and Picea abies in mixed stands
Forest Ecology and Management
(2004) - et al.
Does nitrogen deposition increase forest production? The role of phosphorus
Environmental Pollution
(2010) - et al.
Measurement of microbial biomass phosphorus in soil
Soil Biology and Biochemistry
(1982) - et al.
Measuring rates of gross and net mineralisation of organic phosphorus in soils
Soil Biology and Biochemistry
(2007) - et al.
Dominance of either physicochemical or biological phosphorus cycling processes in temperate forest soils of contrasting phosphate availability
Soil Biology and Biochemistry
(2016) - et al.
Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand
Forest Ecology and Management
(2003)
Competition for inorganic and organic N by blue oak (Quercus douglasii) seedlings, an annual grass, and soil microorganisms in a pot study
Soil Biology and Biochemistry
Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community
Soil Biology and Biochemistry
Microbial biomass and enzyme activities under reduced nitrogen deposition in a spruce forest soil
Applied Soil Ecology
Nitrogen deposition in Swiss forests and its possible relevance for leaf nutrient status, parasite attacks and soil acidification
Environmental Pollution
The fumigation-extraction method to estimate soil microbial biomass: calibration of the KEC value
Soil Biology Biochemistry
Microbially-mediated P fluxes in calcareous soils as a function of water-extractable phosphate
Soil Biology and Biochemistry
Turnover of carbon and phosphorus in the microbial biomass depending on phosphorus availability
Soil Biology and Biochemistry
Microbial gross organic phosphorus mineralization can be stimulated by root exudates – a 33P isotopic dilution study
Soil Biology and Biochemistry
Mineral weathering by bacteria: ecology, actors and mechanisms
Trends Microbiology
An extraction method for measuring soil microbial biomass C
Soil Biology and Biochemistry
Phosphorus availabilities in beech (Fagus sylvatica L.) forests impose habitat filtering on ectomycorrhizal communities and impact tree nutrition
Soil Biology and Biochemistry
Colour Atlas of Ectomycorrhizae
Mechanisms for carbon and nutrient release and retention in beech forest gaps: II the role of soil microbial biomass
Plant and Soil
Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems
Environmental Microbiology
R: a Language and Environment for Statistical Computing
Do nutrient limitation patterns shift from nitrogen toward phosphorus with increasing nitrogen deposition across the northeastern United States?
Ecosystems
Climate change impairs nitrogen cycling in European beech forests
PLoS One
The influence of phosphorus availability and Laccaria bicolor symbiosis on phosphate acquisition, antioxidant enzyme activity, and rhizospheric carbon flux in Populus tremuloides
Mycorrhiza
Spatial and temporal variability of foliar mineral concentration in beech (Fagus sylvatica) stands in northeastern France
Tree Physiology
The role of isotopic techniques on the evaluation of the agronomic effectiveness of P fertilizers
Nutrient Cycling in Agroecosystems
Phosphorus limitation in boreal forests: effects of aluminum and iron accumulation in the humus layer
Ecosystems
Extracellular hydrolytic enzyme profiles of certain South Indian basidiomycetes
African Journal of Biotechnology
Controls on annual nitrogen cycling in the understory of a subarctic birch forest
Ecology
PAST: paleontological statistics software package for education and data analysis
Paleontolology Electronica
Verbessertes Druckaufschlusssystem für biologische und anorganische Materialien
Zeitschrift für Pflanzenernährung und Bodenkunde
Carbon, nitrogen and phosphorus net mineralization in organic horizons of temperate forests: stoichiometry and relations to organic matter quality
Biogeochemistry
Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review
Plant and Soil
Eine photometrische Methode zur Bestimmung der Phosphatase Aktivität in Böden
Zeitschrift für Pflanzenernährung und Bodenkunde
Phosphorus resorption by young beech trees and soil phosphatase activity as dependent on phosphorus availability
Oecologia
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