Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil.

Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km2) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes-urbanization and forest edge creation-on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new "suites" of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction-including increased greenhouse gas production-in temperate forest regions that are subsumed by urban expansion, both now and in the future.

Nitrogen Availability and Microbial Communities of Canopy Soils in a Large Cercidiphyllum japonicum Tree of a Cool-Temperate Old Growth Forest.

Canopy soils on large trees are important for supporting the lives of many canopy plants, and thereby increasing regional biodiversity. However, because of the less accessibility to canopy soils, there is insufficient knowledge on how canopy soils produce available nitrogen (N) for canopy plants through the activity of canopy soil microbes. Canopy soils usually have different soil properties from ground soils, so we hypothesized that canopy soils would have unique microbial communities compared to ground soils, but still provide available N for canopy plants. Here, we compared soil N availability, including net N mineralization and nitrification rate, and microbial communities between canopy soils (organic soils) collected at various heights of a large Cercidiphyllum japonicum tree and ground soils (organic and mineral soils) in a cool-temperate old-growth forest of Japan. The canopy soils had significantly different N availability (mass-based higher but volume-based lower) and microbial communities from the ground mineral soils. Among organic soils, the height of the soil had an impact on the microbial communities but not on the N availability, which agreed with our hypothesis. Despite the decrease in fungal abundance in the higher soils, the increase in certain components of the cellulose-decomposing fungi and oligotrophic bacteria may contribute to the available N production. Also, the abundance of ammonia-oxidizers did not change with the height, which would be important for the nitrification rate. Our study implied canopy soils could provide N to canopy plants partly through the functional redundancy within different microbial communities and constant population of ammonia-oxidizers.

Soil nitrogen cycling is determined by the competition between mycorrhiza and ammonia-oxidizing prokaryotes.

Mycorrhizal fungi have considerable effects on soil carbon (C) storage, as they control the decomposition of soil organic matter (SOM), by modifying the amount of soil nitrogen (N) available for free-living microbes. Through their access to organic N, ectomycorrhizal (ECM) fungi compete with free-living soil microbes; this competition is thought to slow down SOM decomposition. However, arbuscular mycorrhizal (AM) fungi cannot decompose SOM, and therefore must wait for N to first be processed by free-living microbes. It is unclear what form of N the ECM fungi and free-living microbes compete for, or which microbial groups compete for N with ECM fungi. To investigate this, we focused on the N transformation steps (i.e., the degradation of high-molecular-weight organic matter, mineralization, and nitrification) and the microbes driving each step. Simple comparisons between AM forests and ECM forests are not sufficient to assert that mycorrhizal types would determine the N transformation steps in soil, because soil physiochemistry, which strongly affects N transformation steps, differs between the forests. We used an aridity gradient with large differences in soil moisture, pH, and SOM quantity and quality, to distinguish the mycorrhizal and physicochemical effects on N transformation. Soil samples (0-10 cm depth) were collected from AM-symbiotic black locust forests under three aridity levels, and from ECM-symbiotic oak forests under two aridity levels. Soil physicochemical properties, extractable N dynamics and abundance, composition, and function of soil microbial communities were measured. In ECM forests, the ammonia-oxidizing prokaryotic abundance was low, whereas that of ECM fungi was high, resulting in lower nitrate N content than in AM forests. Since ECM forests did not have lower saprotrophic fungal abundance and prokaryotic decompositional activity than the AM forests, the hypothesis that ECM fungi could reduce SOM decay and ammonification by free-living microbes, might not hold in ECM forests. However, the limitation of ECM fungi on nitrate N production would result in a feedback that will accelerate plant dependence on these fungi, thereby raising soil C storage through an increase in the ECM biomass and plant C investment in soils.

Arbuscular Mycorrhizal Community in Roots and Nitrogen Uptake Patterns of Understory Trees Beneath Ectomycorrhizal and Non-ectomycorrhizal Overstory Trees.

Nitrogen (N) is an essential plant nutrient, and plants can take up N from several sources, including via mycorrhizal fungal associations. The N uptake patterns of understory plants may vary beneath different types of overstory trees, especially through the difference in their type of mycorrhizal association (arbuscular mycorrhizal, AM; or ectomycorrhizal, ECM), because soil mycorrhizal community and N availability differ beneath AM (non-ECM) and ECM overstory trees (e.g., relatively low nitrate content beneath ECM overstory trees). To test this hypothesis, we examined six co-existing AM-symbiotic understory tree species common beneath both AM-symbiotic black locust (non-ECM) and ECM-symbiotic oak trees of dryland forests in China. We measured AM fungal community composition of roots and natural abundance stable isotopic composition of N (δ15N) in plant leaves, roots, and soils. The root mycorrhizal community composition of understory trees did not significantly differ between beneath non-ECM and ECM overstory trees, although some OTUs more frequently appeared beneath non-ECM trees. Understory trees beneath non-ECM overstory trees had similar δ15N values in leaves and soil nitrate, suggesting that they took up most of their nitrogen as nitrate. Beneath ECM overstory trees, understory trees had consistently lower leaf than root δ15N, suggesting they depended on mycorrhizal fungi for N acquisition since mycorrhizal fungi transfer isotopically light N to host plants. Additionally, leaf N concentrations in the understory trees were lower beneath ECM than the non-ECM overstory trees. Our results show that, without large differences in root mycorrhizal community, the N uptake patterns of understory trees vary between beneath different overstory trees.