Phosphorus regulates ectomycorrhizal fungi biomass production in a Norway spruce forest

Ectomycorrhizal fungi (EMF) are important components of soil microbial communities, and EMF biomass can potentially increase carbon (C) stocks by accumulating in the soils as necromass and producing recalcitrant structures. EMF growth depends on the C allocated belowground by the host trees, and the nutrient limitation on tree growth is expected to influence this allocation. Therefore, studying EMF production and understanding the factors that regulates it in natural soils are important to understand C cycling in forests.Fungal mycelium collected from ingrowth mesh bags is commonly used to estimate EMF biomass, but these measurements might not reflect the total EMF production since turnover rates of the hyphae are not considered. Here we estimated EMF production and turnover in response to P fertilization (applied as superphosphate) in a Norway spruce forest where nitrogen (N) deposition has resulted in phosphorus (P) limitation of plant production by using a combination of mesh bags with different incubation periods and with Bayesian inferences. To test how localized patches of N and P influence EMF production and turnover we amended some bags with a nitrogen source (methylene urea) or P source (apatite). Additionally, the Bayesian model tested the effect of seasonality (time of mesh-bag harvesting) on EMF production and turnover.We found that turnover of EMF was not affected by P fertilization or mesh-bag amendment. P fertilization had a negative effect on EMF production in all the mesh-bag amendments, suggesting a reduced belowground C allocation to the EMF when P limitation is alleviated. Apatite amendment significantly increased EMF biomass production in comparison with the pure quartz bags in the control plots but not in the P-fertilized plots. This indicates that P-rich patches enhance EMF production in P-limited forests, but not when P is not limiting. Urea amendment had a generally positive effect on EMF production, but this was significantly reduced by P fertilization, suggesting that a decrease in EMF production due to the alleviated P limitation will affect N foraging. Seasonality had a significant effect on EMF production, and the differences registered between the treatments were higher during the warmer months and disappeared at the end of the growing season.Many studies highlight the importance of N for regulating belowground C allocation to EMF in northern coniferous forests, but here we show that the P status of the forest can be equally important for belowground carbon allocation to EMF production in areas with high N deposition

Responses of arbuscular mycorrhizal fungi to long-term inorganic and organic nutrient addition in a lowland tropical forest

Improved understanding of the nutritional ecology of arbuscular mycorrhizal (AM) fungi is important in understanding how tropical forests maintain high productivity on low-fertility soils. Relatively little is known about how AM fungi will respond to changes in nutrient inputs in tropical forests, which hampers our ability to assess how forest productivity will be influenced by anthropogenic change. Here we assessed the influence of long-term inorganic and organic nutrient additions and nutrient depletion on AM fungi, using two adjacent experiments in a lowland tropical forest in Panama. We characterised AM fungal communities in soil and roots using 454-pyrosequencing, and quantified AM fungal abundance using microscopy and a lipid biomarker. Phosphorus and nitrogen addition reduced the abundance of AM fungi to a similar extent, but affected community composition in different ways. Nutrient depletion (removal of leaf litter) had a pronounced effect on AM fungal community composition, affecting nearly as many OTUs as phosphorus addition. The addition of nutrients in organic form (leaf litter) had little effect on any AM fungal parameter. Soil AM fungal communities responded more strongly to changes in nutrient availability than communities in roots. This suggests that the 'dual niches' of AM fungi in soil versus roots are structured to different degrees by abiotic environmental filters, and biotic filters imposed by the plant host. Our findings indicate that AM fungal communities are fine-tuned to nutrient regimes, and support future studies aiming to link AM fungal community dynamics with ecosystem function

Agricultural management practices influence AMF diversity and community composition with cascading effects on plant productivity

Understanding the effects of different agricultural practices on the mycorrhizal symbiosis is important for agricultural production and the sustainable use of soil. We investigated the composition and diversity of arbuscular mycorrhizal fungi (AMF) in soils from fields under different agricultural practices (conventional and organic cereal fields, leys and permanent pastures) in southern Sweden. The diversity of AMF was found to be greatest in permanent pastures, corroborating evidence that agricultural practices such as tillage impair AMF diversity. Neither geographical location nor soil type nor any of the major soil characteristics we measured impacted AMF diversity or community composition. AMF community composition was significantly affected by the different agricultural practices, particularly conventional management, which reduced AMF diversity. Of the cereal fields sampled, those under organic management held the greatest AMF diversity, and in a glasshouse experiment this greater diversity was positively related to barley phosphorus uptake and grain biomass production. Our results demonstrate the impact of different agricultural practices on AMF communities. In particular, we demonstrate the ability of organic farming to sustain greater AMF diversity relative to conventional farming, and the potential importance of this increased diversity for sustainable cereal production

Share the wealth : Trees with greater ectomycorrhizal species overlap share more carbon

The mutualistic symbiosis between forest trees and ectomycorrhizal fungi (EMF) is among the most ubiquitous and successful interactions in terrestrial ecosystems. Specific species of EMF are known to colonize specific tree species, benefitting from their carbon source, and in turn, improving their access to soil water and nutrients. EMF also form extensive mycelial networks that can link multiple root-tips of different trees. Yet the number of tree species connected by such mycelial networks, and the traffic of material across them, are just now under study. Recently we reported substantial belowground carbon transfer between Picea, Pinus, Larix and Fagus trees in a mature forest. Here, we analyze the EMF community of these same individual trees and identify the most likely taxa responsible for the observed carbon transfer. Among the nearly 1,200 EMF root-tips examined, 50%–70% belong to operational taxonomic units (OTUs) that were associated with three or four tree host species, and 90% of all OTUs were associated with at least two tree species. Sporocarp 13C signals indicated that carbon originating from labelled Picea trees was transferred among trees through EMF networks. Interestingly, phylogenetically more closely related tree species exhibited more similar EMF communities and exchanged more carbon. Our results show that belowground carbon transfer is well orchestrated by the evolution of EMFs and tree symbiosis

Ectomycorrhizal community composition and function in a spruce forest transitioning between nitrogen and phosphorus limitation

Nitrogen is the main limiting nutrient in boreal ecosystems, but studies in southwest Sweden suggest that certain forests approach phosphorus (P) limitation driven by nitrogen (N) deposition. We added N, P or N + P to a Norway spruce forest in this region, to push the system to N or P limitation. Tree growth and needle nutrient concentrations indicated that the trees are P limited. EMF biomass was reduced only by N + P additions. Soil EMF communities responded more strongly to P than to N. Addition of apatite to ingrowth meshbags altered EMF community composition and enhanced the abundance of Imleria badia in the control and N plots, but not when P was added. The ecological significance of this species is discussed. Effects on tree growth, needle chemistry, and EMF communities indicate a dynamic interaction between EMF fungi and the nutrient status of trees and soils

Anthropogenic nitrogen enrichment increased the efficiency of belowground biomass production in a boreal forest

Anthropogenic nitrogen (N) enrichment in boreal forests has been shown to enhance aboveground net primary production and downregulate soil respiration, but it is not well understood if these effects are driven by reduced belowground C allocation or shifts between biomass production and respiration in fine-roots and ectomycorrhizal fungi (EMF). We utilized an experiment in a Pinus sylvestris (L.) forest simulating anthropogenic N enrichment with additions of low (3, 6, and 12 kg N ha−1 yr−1) and high (50 kg N ha−1 yr−1 × 12 yr) doses of N (n = 6) and measured the production of needles, fine-roots, and EMF mycelium during the 12th and 13th year of the experiment. We created a biomass production efficiency index by relating the biomass production rate to root-associated respiration, including both root and EMF respiration. The high N treatment enhanced the production of both needles and fine-roots, with a relatively larger increase in fine-roots, and strongly increased fine-root biomass production efficiency but had no effect on the fungal biomass in fine-roots or the production of EMF mycelium. The low N treatments had no effect on any of the measured variables. These results show that high levels of N enrichment drive shifts in the use of C allocated below ground, with less C going towards metabolic functions that result in rapid C emissions, and more C going towards the production of new tissues

Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange

Agricultural fertilization significantly affects arbuscular mycorrhizal fungal (AMF) community composition. However, the functional implications of community shifts are unknown, limiting understanding of the role of AMF in agriculture. We assessed AMF community composition at four sites managed under the same nitrogen (N) and phosphorus (P) fertilizer regimes for 55�yr. We also established a glasshouse experiment with the same soils to investigate AMF–barley (Hordeum vulgare) nutrient exchange, using carbon (C) and P isotopic labelling. N fertilization affected AMF community composition, reducing diversity; P had no effect. In the glasshouse, AMF contribution to plant P declined with P fertilization, but was unaffected by N. Barley C allocation to AMF also declined with P fertilization. As N fertilization increased, C allocation to AMF per unit of P exchanged increased. This occurred with and without P fertilization, and was concomitant with reduced barley biomass. AMF community composition showed no relationship with glasshouse experiment results. The results indicate that plants can reduce C allocation to AMF in response to P fertilization. Under N fertilization, plants allocate an increasing amount of C to AMF and receive relatively less P. This suggests an alteration in the terms of P–C exchange under N fertilization regardless of soil P status

The role of phosphorus, magnesium and potassium availability in soil fungal exploration of mineral nutrient sources in Norway spruce forests

We investigated fungal growth and community composition in buried meshbags, amended with apatite, biotite or hornblende, in Norway spruce (Picea abies) forests of varying nutrient status. Norway spruce needles and soil collected from forests overlying serpentinite had low levels of potassium and phosphorus, those from granite had low levels of magnesium, whereas those from amphibolite had comparably high levels of these nutrients. We assayed the fungal colonization of meshbags by measuring ergosterol content and fungal community with 454 sequencing of the internal transcribed spacer region. In addition, we measured fine root density. Fungal biomass was increased by apatite amendment across all plots and particularly on the K- and P-deficient serpentinite plots, whereas hornblende and biotite had no effect on fungal biomass on any plots. Fungal community (total fungal and ectomycorrhizal) composition was affected strongly by sampling location and soil depth, whereas mineral amendments had no effect on community composition. Fine root biomass was significantly correlated with fungal biomass. Ectomycorrhizal communities may respond to increased host-tree phosphorus demand by increased colonization of phosphorus-containing minerals, but this does not appear to translate to a shift in ectomycorrhizal community composition. This growth response to nutrient demand does not appear to exist for potassium or magnesium limitation

Nitrophobic ectomycorrhizal fungi are associated with enhanced hydrophobicity of soil organic matter in a Norway spruce forest

In boreal forests an important part of the photo assimilates are allocated belowground to support symbiosis of ectomycorrhizal fungi (EMF). The production of EMF extramatrical mycelium can contribute to carbon (C) sequestration in soils, but the extent of this contribution depends on the composition of the EMF community. Some species can decrease soil C stocks by degrading soil organic matter (SOM), and certain species may enhance soil C stocks by producing hydrophobic mycelia which can reduce the rate of SOM decomposition. To test how EMF communities contribute to the development of hydrophobicity in SOM, we incubated sand-filled fungal-ingrowth mesh bags amended with maize compost for one, two or three growing seasons in non-fertilized and fertilized plots in a young Norway spruce (Picea abies) forest. We measured hydrophobicity as determined by the contact angle and the C/N ratios in the mesh bags contents along with the amount of new C entering the mesh bags from outside (determined by C3 input to C4 substrate), and related that to the fungal community composition. The proportion of EMF species increased over time to become the dominant fungal guild after three growing seasons. Fertilization significantly reduced fungal growth and altered EMF communities. In the control plots the most abundant EMF species was Piloderma olivaceum, which was absent in the fertilized plots. The hydrophobicity of the mesh bag contents reached the highest values after three growing seasons only in the unfertilized controls plots and was positively related to the abundance of P. olivaceum, the C/N ratios of the mesh bag contents and the amount of new C in the mesh bags. These results suggest that some EMF species are associated with higher hydrophobicity of SOM and that EMF community shifts induced by fertilization may result in reduced hydrophobicity of soil organic matter, which in turn may reduce C sequestration rates