Recent advances in exploring physiology and biodiversity of ectomycorrhizas highlight the functioning of these symbioses in ecosystems

Ectomycorrhizas, the dominating mycorrhizal symbiosis in boreal, temperate and some tropical forests, are formed by 5000-6000 species of the asco- and basidiomycetes. This high diversity of fungal partners allows optimal foraging and mobilisation of various nitrogen and phosphorus forms from organic soil layers. In this review, two approaches to study the functioning of this multitude of symbiotic associations are presented. On selected culture models, physiological and molecular investigations have shown that the supply of hexoses has a key function in controlling the plant^fungus interaction via partner-specific regulation of gene expression. Environmental factors which affect fungal carbon supply, such as increased nitrogen availability, also affect mycorrhiza formation. Based on such laboratory results, the adaptative capability of ectomycorrhizas to changing field conditions is discussed. The second approach consists of analysing the distribution of mycorrhizas in ecosystem compartments and to relate distribution patterns to variations of ecological factors. Recent advances in identification of fungal partners in ectomycorrhizas by analysing the internal transcribed spacer of ribosomal DNA are presented, which can help to resolve sampling problems in field studies. The limits of the laboratory and the field approaches are discussed. Despite some problems, this combined approach is the most promising. Direct investigation of gene expression, which has been introduced for soil bacteria, will be difficult in the case of mycorrhizal fungi which constitute organisms with functionally varying structure

Temporal Changes and Alternating Host Tree Root and Shoot Growth Affect Soil Microbiomes

Patterns of trees’ endogenous rhythmic growth (ERG) and paralleled C allocation shift between root and shoot systems have been studied, but there is still a need to understand their impact in shaping soil microbiomes. Moreover, the impact of plants on soil microbial communities can be modulated or overweighed by time-induced plant and/or seasonal changes. Thus, we intended to analyze the structure of soil microbiomes as response to simultaneous alternated host tree root and shoot flushes and time-induced changes within one vegetation period at two sites in Central Germany. In this study, we utilized oak phytometers (Quercus robur L., clone DF159) as host trees, and made use of their ERG, whereby consecutive root and shoot flushes make a complete growth cycle. We studied two complete growth cycles during the same vegetation period, performed a non-destructive soil sampling and applied high-throughput amplicon sequencing of the bacterial 16S gene and the fungal ITS2 region. As C allocation shifts between the tree root and shoot, released root exudates and consequently the nutrient availability alternate for soil microorganisms. We therefore anticipated different microbial communities in the host tree root zone along the growth cycles until autumnal leaf senescence. In our results, the bacterial community exhibited a directional change over time along the vegetation period. In contrast, the fungal community appeared sample specific. Our findings enlarge the current understanding of the temporal microbial assembly in the host tree root zone

Tree Root Zone Microbiome: Exploring the Magnitude of Environmental Conditions and Host Tree Impact

Tree roots attract their associated microbial partners from the local soil community. Accordingly, tree root-associated microbial communities are shaped by both the host tree and local environmental variables. To rationally compare the magnitude of environmental conditions and host tree impact, the “PhytOakmeter” project planted clonal oak saplings (Quercus robur L., clone DF159) as phytometers into different field sites that are within a close geographic space across the Central German lowland region. The PhytOakmeters were produced via micro-propagation to maintain their genetic identity. The current study analyzed the microbial communities in the PhytOakmeter root zone vs. the tree root-free zone of soil two years after out-planting the trees. Soil DNA was extracted, 16S and ITS2 genes were respectively amplified for bacteria and fungi, and sequenced using Illumina MiSeq technology. The obtained microbial communities were analyzed in relation to soil chemistry and weather data as environmental conditions, and the host tree growth. Although microbial diversity in soils of the tree root zone was similar among the field sites, the community structure was site-specific. Likewise, within respective sites, the microbial diversity between PhytOakmeter root and root-free zones was comparable. The number of microbial species exclusive to either zone, however, was higher in the host tree root zone than in the tree root-free zone. PhytOakmeter “core” and “site-specific” microbiomes were identified and attributed to the host tree selection effect and/or to the ambient conditions of the sites, respectively. The identified PhytOakmeter root zone-associated microbiome predominantly included ectomycorrhizal fungi, yeasts and saprotrophs. Soil pH, soil organic matter, and soil temperature were significantly correlated with the microbial diversity and/or community structure. Although the host tree contributed to shape the soil microbial communities, its effect was surpassed by the impact of environmental factors. The current study helps to understand site-specific microbe recruitment processes by young host trees

Balance between geographic, soil, and host tree parameters to shape soil microbiomes associated to clonal oak varies across soil zones along a European North–South transect

Tree root-associated microbiomes are shaped by geographic, soil physico-chemical, and host tree parameters. However, their respective impacts on microbiome variations in soils across larger spatial scales remain weakly studied. We out-planted saplings of oak clone DF159 (Quercus robur L.) as phytometer in four grassland field sites along a European North–South transect. After four years, we first compared the soil microbiomes of the tree root zone (RZ) and the tree root-free zone (RFZ). Then, we separately considered the total microbiomes of both zones, besides the microbiome with significant affinity to the RZ and compared their variability along the transect. Variations within the microbiome of the tree RFZ were shaped by geographic and soil physico-chemical changes, whereby bacteria responded more than fungi. Variations within both microbiomes of the tree RZ depended on the host tree and abiotic parameters. Based on perMANOVA and Mantel correlation tests, impacts of site specificities and geographic distance strongly decreased for the tree RZ affine microbiome. This pattern was more pronounced for fungi than bacteria. Shaping the microbiome of the soil zones in root proximity might be a mechanism mediating the acclimation of oaks to a wide range of environmental conditions across geographic regions

Unraveling spatiotemporal variability of arbuscular mycorrhizal fungi in a temperate grassland plot

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Goldmann, K., Boeddinghaus, R. S., Klemmer, S., Regan, K. M., Heintz-Buschart, A., Fischer, M., Prati, D., Piepho, H., Berner, D., Marhan, S., Kandeler, E., Buscot, F., & Wubet, T. Unraveling spatiotemporal variability of arbuscular mycorrhizal fungi in a temperate grassland plot. Environmental Microbiology, 22(3),(2020): 873-888, doi:10.1111/1462-2920.14653.Soils provide a heterogeneous environment varying in space and time; consequently, the biodiversity of soil microorganisms also differs spatially and temporally. For soil microbes tightly associated with plant roots, such as arbuscular mycorrhizal fungi (AMF), the diversity of plant partners and seasonal variability in trophic exchanges between the symbionts introduce additional heterogeneity. To clarify the impact of such heterogeneity, we investigated spatiotemporal variation in AMF diversity on a plot scale (10 × 10 m) in a grassland managed at low intensity in southwest Germany. AMF diversity was determined using 18S rDNA pyrosequencing analysis of 360 soil samples taken at six time points within a year. We observed high AMF alpha‐ and beta‐diversity across the plot and at all investigated time points. Relationships were detected between spatiotemporal variation in AMF OTU richness and plant species richness, root biomass, minimal changes in soil texture and pH. The plot was characterized by high AMF turnover rates with a positive spatiotemporal relationship for AMF beta‐diversity. However, environmental variables explained only ≈20% of the variation in AMF communities. This indicates that the observed spatiotemporal richness and community variability of AMF was largely independent of the abiotic environment, but related to plant properties and the cooccurring microbiome.We thank the managers of the three Exploratories, Kirsten Reichel‐Jung, Swen Renner, Katrin Hartwich, Sonja Gockel, Kerstin Wiesner, and Martin Gorke for their work in maintaining the plot and project infrastructure; Christiane Fischer and Simone Pfeiffer for giving support through the central office, Michael Owonibi and Andreas Ostrowski for managing the central data base, and Eduard Linsenmair, Dominik Hessenmöller, Jens Nieschulze, Ernst‐Detlef Schulze, Wolfgang W. Weisser and the late Elisabeth Kalko for their role in setting up the Biodiversity Exploratories project. The work has been funded by the DFG Priority Program 1374 ‘Infrastructure‐Biodiversity‐Exploratories’ (BU 941/22‐1, BU 941/22‐3, KA 1590/8‐2, KA 1590/8‐3). Field work permits were issued by the responsible state environmental office of Baden‐Württemberg (according to § 72 BbgNatSchG). Likewise, we kindly thank Beatrix Schnabel, Melanie Günther and Sigrid Härtling for 454 sequencing in Halle. AHB gratefully acknowledges the support of the German Centre for Integrative Biodiversity Research (iDiv) Halle‐Jena‐Leipzig funded by the German Research Foundation (FZT 118). Authors declare no conflict of interests

Experimental Evidence of Functional Group-Dependent Effects of Tree Diversity on Soil Fungi in Subtropical Forests

Deconvoluting the relative contributions made by specific biotic and abiotic drivers to soil fungal community compositions facilitates predictions about the functional responses of ecosystems to environmental changes, such as losses of plant diversity, but it is hindered by the complex interactions involved. Experimental assembly of tree species allows separation of the respective effects of plant community composition (biotic components) and soil properties (abiotic components), enabling much greater statistical power than can be achieved in observational studies. We therefore analyzed these contributions by assessing, via pyrotag sequencing of the internal transcribed spacer (ITS2) rDNA region, fungal communities in young subtropical forest plots included in a large experiment on the effects of tree species richness. Spatial variables and soil properties were the main drivers of soil fungal alpha and beta-diversity, implying strong early-stage environmental filtering and dispersal limitation. Tree related variables, such as tree community composition, significantly affected arbuscular mycorrhizal and pathogen fungal community structure, while differences in tree host species and host abundance affected ectomycorrhizal fungal community composition. At this early stage of the experiment, only a limited amount of carbon inputs (rhizodeposits and leaf litter) was being provided to the ecosystem due to the size of the tree saplings, and persisting legacy effects were observed. We thus expect to find increasing tree related effects on fungal community composition as forest development proceeds

Land-Use Intensity Rather Than Plant Functional Identity Shapes Bacterial and Fungal Rhizosphere Communities

The rhizosphere encompasses the soil surrounding the surface of plants’ fine roots. Accordingly, the microbiome present is influenced by both soil type and plant species. Furthermore, soil microbial communities respond to land-use intensity due to the effects on soil conditions and plant performance. However, there is limited knowledge about the impact of grassland management practices under field conditions on the composition of both bacteria and fungi in the rhizosphere of different plant functional groups. In spring 2014 we planted four phytometer species, two forbs (Plantago lanceolata, Achillea millefolium) and two grasses (Dactylis glomerata, Arrhenatherum elatius) into 13 permanent experimental grassland plots, differing in management. After 6 months, rhizosphere and bulk soil associated with the phytometer plants were sampled, microbial genomic DNA was extracted and bacterial 16S and fungal ITS rDNA were sequenced using Illumina MiSeq. Our study revealed that the rhizosphere microbial community was more diverse than the bulk soil community. There were no differences in microbial community composition between the two plant functional groups, but a clear impact of root traits and edaphic conditions. Land-use intensity strongly affected plant productivity, neighboring plant richness and edaphic conditions, especially soil C/N ratio, which in turn had a strong influence on root traits and thereby explained to large extent microbial community composition. Rhizosphere microbes were mainly affected by abiotic factors, in particular by land-use intensity, while plant functional type had only subordinate effects. Our study provides novel insights into the assembly of rhizosphere bacterial and fungal communities in response to land-use intensity and plant functional groups in managed grassland ecosystems

Organic agricultural practice enhances arbuscular mycorrhizal symbiosis in correspondence to soil warming and altered precipitation patterns

Climate and agricultural practice interact to influence both crop production and soil microbes in agroecosystems. Here, we carried out a unique experiment in Central Germany to simultaneously investigate the effects of climates (ambient climate vs. future climate expected in 50–70 years), agricultural practices (conventional vs. organic farming), and their interaction on arbuscular mycorrhizal fungi (AMF) inside wheat (Triticum aestivum L.) roots. AMF communities were characterized using Illumina sequencing of 18S rRNA gene amplicons. We showed that climatic conditions and agricultural practices significantly altered total AMF community composition. Conventional farming significantly affected the AMF community and caused a decline in AMF richness. Factors shaping AMF community composition and richness at family level differed greatly among Glomeraceae, Gigasporaceae and Diversisporaceae. An interactive impact of climate and agricultural practices was detected in the community composition of Diversisporaceae. Organic farming mitigated the negative effect of future climate and promoted total AMF and Gigasporaceae richness. AMF richness was significantly linked with nutrient content of wheat grains under both agricultural practices

The multidimensionality of soil macroecology

The recent past has seen a tremendous surge in soil macroecological studies and new insights into the global drivers of one‐quarter of the biodiversity of the Earth. Building on these important developments, a recent paper in Global Ecology and Biogeography outlined promising methods and approaches to advance soil macroecology. Among other recommendations, White and colleagues introduced the concept of a spatial three‐dimensionality in soil macroecology by considering the different spheres of influence and scales, as soil organism size ranges vary from bacteria to macro‐ and megafauna. Here, we extend this concept by discussing three additional dimensions (biological, physical, and societal) that are crucial to steer soil macroecology from pattern description towards better mechanistic understanding. In our view, these are the requirements to establish it as a predictive science that can inform policy about relevant nature and management conservation actions. We highlight the need to explore temporal dynamics of soil biodiversity and functions across multiple temporal scales, integrating different facets of biodiversity (i.e., variability in body size, life‐history traits, species identities, and groups of taxa) and their relationships to multiple ecosystem functions, in addition to the feedback effects between humans and soil biodiversity. We also argue that future research needs to consider effective soil conservation policy and management in combination with higher awareness of the contributions of soil‐based nature's contributions to people. To verify causal relationships, soil macroecology should be paired with local and globally distributed experiments. The present paper expands the multidimensional perspective on soil macroecology to guide future research contents and funding. We recommend considering these multiple dimensions in projected global soil biodiversity monitoring initiatives