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Spatial and temporal processes shaping microbial communities are inseparably linked but rarely studied together. By Illumina 16S rRNA sequencing, we monitored soil bacteria in 360 stations on a 100 square meter plot distributed across six intra-annual samplings in a rarely managed, temperate grassland. Using a multi-tiered approach, we tested the extent to which stochastic or deterministic processes influenced the composition of local communities. A combination of phylogenetic turnover analysis and null modeling demonstrated that either homogenization by unlimited stochastic dispersal or scenarios, in which neither stochastic processes nor deterministic forces dominated, explained local assembly processes. Thus, the majority of all sampled communities (82%) was rather homogeneous with no significant changes in abundance-weighted composition. However, we detected strong and uniform taxonomic shifts within just nine samples in early summer. Thus, community snapshots sampled from single points in time or space do not necessarily reflect a representative community state. The potential for change despite the overall homogeneity was further demonstrated when the focus shifted to the rare biosphere. Rare OTU turnover, rather than nestedness, characterized abundance-independent β-diversity. Accordingly, boosted generalized additive models encompassing spatial, temporal and environmental variables revealed strong and highly diverse effects of space on OTU abundance, even within the same genus. This pure spatial effect increased with decreasing OTU abundance and frequency, whereas soil moisture – the most important environmental variable – had an opposite effect by impacting abundant OTUs more than the rare ones. These results indicate that – despite considerable oscillation in space and time – the abundant and resident OTUs provide a community backbone that supports much higher β-diversity of a dynamic rare biosphere. Our findings reveal complex interactions among space, time, and environmental filters within bacterial communities in a long-established temperate grassland.

Journal of Ecology, 107 (S 5), ISSN:0022-0477

Grassland ecosystems provide a wide range of services to human societies (Allan et al., 2015) and plants and soil microorganisms have been identified as key drivers of ecosystem functioning (Soliveres et al., 2016). Therefore, understanding soil microbial distributions and processes in agricultural grassland soils is crucial for characterizing these ecosystems and for predicting how they may shift in a changing environment. Yet we are only beginning to understand these complex ecosystems, which account for about 26% of the world’s terrestrial surface (FAOSTATS, 2018), making it especially urgent to gain better insights into the effects of land-use intensity on soil microbial properties and plant-microbe interactions. This thesis was conducted to evaluate the impact land-use intensity has on soil microbial biogeography of grasslands with respect to both spatial patterns and temporal changes in soil microbial abundance, function (in terms of enzyme activities), and community composition. It also investigated the relationships between plants and the spatial and temporal distributions of soil microorganisms. Thereby both, land-use intensity effects and plant-microbe interactions, were assessed in light of ecological niche and neutral theory. This thesis is based on three observational studies conducted on from one to 150 continuously farmed, un-manipulated grassland sites in three regions of Germany within the Biodiversity Exploratories project (DFG priority program 1374). The first study assessed the effects of land-use intensity and physico-chemical soil properties on the spatial biogeography of soil microbial abundance and function in 18 grasslands sites from two of the three regions, sampled at one time point. The second study analyzed spatial and temporal distributions of alpha- and beta-diversity of arbuscular mycorrhizal fungi in a low land-use intensity grassland with six sampling time points across one season. The third study investigated both legacy and short-term change effects of land-use intensity, soil physico-chemical properties, plant functional traits, and plant biomass properties on temporal changes in soil microbial abundance, function, and community composition in 150 grassland sites across three regions, with particular regard to direct and indirect land-use intensity effects. Although the three studies used different approaches and assessed different soil microbial properties, general patterns were detectable. Abiotic soil properties, namely pH, nitrogen content, texture, and bulk density played fundamental roles for spatial and temporal microbial biogeography. Since these factors were specific and unique for each investigated site, they formed the background based on which other processes occurred. In addition to abiotic soil properties, impacts of land-use intensity and plants were detected, though to various degrees in the three studies. Land-use intensity played a much smaller role than anticipated in the first and third study. No influence on the spatial distribution of soil microbial abundance and function could be detected in the first study. In the third study, short-term changes in and legacy effects of land-use intensity played a minor role with respect to short-term changes in soil microbial abundance, function, and community composition. Where detected, changes in land-use intensity had a direct and negative effect on soil microbial properties in structural equation modelling; i.e., increases in land-use intensity reduced, e.g., soil microbial enzyme activities, while legacy effects of land-use intensity were shown to act both directly and indirectly on soil microbial properties. Thereby indirect legacy effects were mediated via plant functional traits. Only one of the three studies detected minor plant diversity effects on soil microbial properties. Instead, functional properties of the plant communities, i.e., plant functional traits, biomass, and nutritional quality, were significantly related to spatial and temporal distributions of soil microorganisms. Finally, the findings of the three studies suggest that processes related to niche and neutral theory both drive spatial and temporal patterns of soil microbial properties at the investigated plot scale (up to 50 m × 50 m). This thesis concluded that in order to gain deeper insights into the complex functions and processes occurring in grassland ecosystems, a multidisciplinary approach investigating fundamental physico-chemical site characteristics, microbial soil properties, and plants is necessary. The results of the thesis suggest that focus be turned to functional properties of plant and microbial communities, as they are closely intermingled, provide more detailed insights into plant-microbe interactions, and are able to reflect effects of human impacts on grassland soils better than diversity measures. Die vorliegende Dissertation diente dem Zweck, die Einflüsse der Landnutzungsintensität von Grünländern auf die Biogeographie von Bodenmikroorganismen in Bezug auf die räumliche Verteilung und zeitliche Veränderung von mikrobieller Biomasse, Funktion und Gemeinschaftsstrukturen aufzudecken und die Beziehungen zwischen Pflanzen und den räumlichen und zeitlichen Verteilungsmustern von Bodenmikroorganismen zu untersuchen. Dabei wurde auch betrachtet, inwieweit die Verteilung der Mikroorganismen den Konzepten der ökologischen Nischen- und Neutraltheorie entspricht. Die Dissertation basiert auf drei beobachtenden Studien, die auf einer bis 150 dauerhaft bewirtschafteten und nicht manipulierten Grünlandflächen durchgeführt wurden. Die Flächen sind verteilt auf drei Regionen in Deutschland und Teil des Schwerpunktforschungsprogramms Biodiversitäts-Exploratorien der Deutschen Forschungsgemeinschaft (DFG 1374). Die erste Studie untersuchte die Effekte von Landnutzungsintensität und physikalisch-chemischen Bodeneigenschaften auf die räumliche Biogeographie von mikrobieller Biomasse und Funktion zu einem einzelnen Zeitpunkt in 18 Grünlandflächen, die auf zwei Regionen verteilt sind. Die zweite Studie analysierte die räumliche und zeitliche Verteilung der Alpha- und Betadiversität arbuskulärer Mykorrhizapilze (AMF) in einem extensiv genutzten Grünland mittels sechs Probennahmezeitpunkten verteilt über die Vegetationsperiode eines Jahres. Die dritte Studie untersuchte sogenannte „Legacy“ und kurzfristige Effekte von veränderter Landnutzungsintensität, physikalisch-chemischen Bodeneigenschaften, funktionellen Pflanzeneigenschaften und Charakteristika der pflanzlichen Biomasse auf zeitliche Veränderungen von mikrobieller Biomasse, Funktion und Gemeinschaftsstruktur in 150 Grünlandböden verteilt auf drei Regionen, sowie direkte und indirekte Effekte der Landnutzungsintensität. Obwohl alle drei Studien unterschiedliche Ansätze verfolgten und verschiedene bodenmikrobielle Eigenschaften untersuchten, sind generelle Muster erkennbar: abiotische Bodeneigenschaften, namentlich pH-Wert, Stickstoffgehalt, Textur und Lagerungsdichte, waren für die räumliche und zeitliche Biogeographie der Bodenmikroorganismen von fundamentaler Bedeutung. Sie waren spezifisch für jede der untersuchten Flächen und bildeten den Hintergrund, vor dem sich andere Prozesse abspielten. Zusätzlich zu den abiotischen Bodeneigenschaften wurden, wenn auch in unterschiedlichem Maße, Einflüsse von Landnutzungsintensität und Pflanzen in den drei Studien detektiert. Die Landnutzungsintensität spielte dabei eine wesentlich geringere Rolle als ursprünglich angenommen. Sie hatte keinen Einfluss auf die räumliche Verteilung der bodenmikrobiellen Biomasse oder Funktion in der ersten Studie. In der dritten Studie waren kurzfristige Veränderungen und Legacy-Effekte nur in geringem Maße mit kurzfristigen Veränderungen von bodenmikrobieller Biomasse, Funktion und Gemeinschaftsstruktur assoziiert. Die Strukturgleichungsmodelle zeigen, dass sich die Effekte von kurzfristigen Veränderung der Landnutzungsintensität, dort wo sie auftraten, direkt und negative auf die kurzfristigen Veränderungen bodenmikrobieller Eigenschaften auswirkten. Dahingegen wirkten sich Legacy-Effekte der Landnutzungsintensität sowohl direkt als auch indirekt auf bodenmikrobielle Eigenschaften aus. Die indirekten Legacy-Effekte wurden dabei über funktionelle Pflanzeneigenschaften auf die Mikroorganismen übertragen. Nur eine der drei Studien fand einen marginalen Einfluss der Pflanzendiversität auf die bodenmikrobiellen Eigenschaften. Stattdessen waren funktionelle Eigenschaften der Pflanzengemeinschaften sowie deren Biomasse und Futterqualität signifikant mit der räumlichen und zeitlichen Verteilung von Bodenmikroorganismen verbunden. In Bezug auf die Nischen- und Neutraltheorie sprechen die Ergebnisse der drei Studien dafür, dass sowohl Prozesse, die mit der Nischentheorie zusammenhängen, als auch solche, die mit der Neutraltheorie in Verbindung stehen, die räumliche und zeitliche Verteilung von bodenmikrobiellen Eigenschaften auf der untersuchten Plotskala (bis 50 m × 50 m) steuern. Diese Dissertation zieht die Schlussfolgerung, dass multidisziplinäre Forschung notwendig ist, um die komplexen Funktionen und Prozesse von Grünlandökosystemen zu erforschen. Diese müssen sowohl die fundamentalen physikalischen und chemischen Eigenschaften der Böden, als auch die Eigenschaften der Bodenmikroorganismen und Pflanzengemeinschaften umfassen. Dabei sprechen die Ergebnisse dieser Arbeit dafür, dass ein besonderes Augenmerk auf die funktionellen Eigenschaften von Pflanzen- und Mikrobengemeinschaften gelegt werden sollte, da diese eng miteinander verflochten sind und bessere Einblicke in die Interaktionen zwischen Pflanzen und Mikroorganismen gewähren sowie besser in der Lage sind die Effekte von menschlichen Einflüssen auf Grünlandböden wieder zu spiegeln, als die bisher oft üblichen Diversitätsmessungen.

Increased warming in spring and prolonged summer drought may alter soil microbial denitrification. We measured potential denitrification activity and denitrifier marker gene abundances (nirK, nirS, nosZ) in grasslands soils in three geographic regions characterized by site-specific land-use indices (LUI) after warming in spring, at an intermediate sampling and after summer drought. Potential denitrification was significantly increased by warming, but did not persist over the intermediate sampling. At the intermediate sampling, the relevance of grassland land-use intensity was reflected by increased potential N2O production at sites with higher LUI. Abundances of total bacteria did not respond to experimental warming or drought treatments, displaying resilience to minor and short-term effects of climate change. In contrast, nirS- and nirK-type denitrifiers were more influenced by drought in combination with LUI and pH, while the nosZ abundance responded to the summer drought manipulation. Land-use was a strong driver for potential denitrification as grasslands with higher LUI also had greater potentials for N2O emissions. We conclude that both warming and drought affected the denitrifying communities and the potential denitrification in grassland soils. However, these effects are overruled by regional and site-specific differences in soil chemical and physical properties which are also related to grassland land-use intensity

Evidence from experimental and established grasslands indicates that plant biodiversity can modify the water cycle. One suspected mechanism behind this is a higher infiltration capacity (ν$_{B}$) and hydraulic conductivity (K) of the soil on species-rich grasslands. However, in established and agriculturally managed grasslands, biodiversity effects cannot be studied independent of land-use effects. Therefore, we investigated in established grassland systems how land-use intensity and associated biodiversity of plants and soil animals affect νB and K at and close to saturation. On 50 grassland plots along a land-use intensity gradient in the Biodiversity Exploratory Schwäbische Alb, Germany, we measured νB with a hood infiltrometer at several matrix potentials and calculated the saturated and unsaturated K. We statistically analysed the relationship between ν$_{B}$ or K and land-use information (e.g., fertilising intensity), abiotic (e.g., soil texture) and biotic data (e.g., plant species richness, earthworm abundance). Land-use intensity decreased and plant species richness increased ν$_{B}$ and K, while the direction of the effects of soil animals was inconsistent. The effect of land-use intensity on ν$_{B}$ and K was mainly attributable to its negative effect on plant species richness. Our results demonstrate that plant species richness was a better predictor of ν$_{B}$ and K at and close to saturation than land-use intensity or soil physical properties in the established grassland systems of the Schwäbische Alb.

Land-use intensification can increase provisioning ecosystem services, such as food and timber production, but it also drives changes in ecosystem functioning and biodiversity loss, which may ultimately compromise human wellbeing. To understand how changes in land-use intensity affect the relationships between biodiversity, ecosystem functions, and services, we built networks from correlations between the species richness of 16 trophic groups, 10 ecosystem functions, and 15 ecosystem services. We evaluated how the properties of these networks varied across land-use intensity gradients for 150 forests and 150 grasslands. Land-use intensity significantly affected network structure in both habitats. Changes in connectance were larger in forests, while changes in modularity and evenness were more evident in grasslands. Our results show that increasing land-use intensity leads to more homogeneous networks with less integration within modules in both habitats, driven by the belowground compartment in grasslands, while forest responses to land management were more complex. Land-use intensity strongly altered hub identity and module composition in both habitats, showing that the positive correlations of provisioning services with biodiversity and ecosystem functions found at low land-use intensity levels, decline at higher intensity levels. Our approach provides a comprehensive view of the relationships between multiple components of biodiversity, ecosystem functions, and ecosystem services and how they respond to land use. This can be used to identify overall changes in the ecosystem, to derive mechanistic hypotheses, and it can be readily applied to further global change drivers.