Significance Biological diversity is the foundation for the maintenance of ecosystems. Consequently it is thought that anthropogenic activities that reduce the diversity in ecosystems threaten ecosystem performance. A large proportion of the biodiversity within terrestrial ecosystems is hidden below ground in soils, and the impact of altering its diversity and composition on the performance of ecosystems is still poorly understood. Using a novel experimental system to alter levels of soil biodiversity and community composition, we found that reductions in the abundance and presence of soil organisms results in the decline of multiple ecosystem functions, including plant diversity and nutrient cycling and retention. This suggests that below-ground biodiversity is a key resource for maintaining the functioning of ecosystems.

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N 2 O is a potent greenhouse gas involved in the destruction of the protective ozone layer in the stratosphere and contributing to global warming. The ecological processes regulating its emissions from soil are still poorly understood. Here, we show that the presence of arbuscular mycorrhizal fungi (AMF), a dominant group of soil fungi, which form symbiotic associations with the majority of land plants and which influence a range of important ecosystem functions, can induce a reduction in N 2 O emissions from soil. To test for a functional relationship between AMF and N 2 O emissions, we manipulated the abundance of AMF in two independent greenhouse experiments using two different approaches (sterilized and re-inoculated soil and non-mycorrhizal tomato mutants) and two different soils. N 2 O emissions were increased by 42 and 33% in microcosms with reduced AMF abundance compared to microcosms with a well-established AMF community, suggesting that AMF regulate N 2 O emissions. This could partly be explained by increased N immobilization into microbial or plant biomass, reduced concentrations of mineral soil N as a substrate for N 2 O emission and altered water relations. Moreover, the abundance of key genes responsible for N 2 O production (nirK) was negatively and for N 2 O consumption (nosZ) positively correlated to AMF abundance, indicating that the regulation of N 2 O emissions is transmitted by AMF-induced changes in the soil microbial community. Our results suggest that the disruption of the AMF symbiosis through intensification of agricultural practices may further contribute to increased N 2 O emissions.

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Summary1. Efficient resource use is a key factor for sustainable production and a necessity for meeting future global food demands. However, the factors that control resource use efficiency in agro-ecosystems are only partly understood. 2. We investigated the influence of soil biota on nutrient leaching, nutrient-use efficiency and plant performance in outdoor, open-top lysimeters comprising a volume of 230 L. The lysimeters were filled with sterilized soil in two horizons and inoculated with a reduced soil-life inoculum (soil biota ≤11 lm, microbially dominated) and an enriched soil-life inoculum [soil organisms ≤2 mm, also containing arbuscular mycorrhizal fungi (AMF)]. A crop rotation was planted, and nutrient leaching losses, plant biomass and nutrient contents were assessed over a period of almost 2 years. 3. In the first year of the experiment, enriched soil life increased crop yield (+22%), N uptake (+29%) and P uptake (+110%) of maize and strongly reduced leaching losses of N (À51%, corresponding to a reduction of 76 kg N ha À1 ). In the second year, wheat biomass (+17%) and P contents (+80%) were significantly increased by enriched soil life, but the differences were lower than in the first year. 4. Enriched soil life also increased P mobilization from soil (+112%) and significantly reduced relative P leaching losses (À25%), defined as g P leached per kg P plant uptake, as well as relative N leaching losses (À36%), defined as kg N leached per kg N plant uptake, demonstrating that nutrient-use efficiency was increased in the enriched soil-life treatment. 5. Synthesis and applications. Soil biota are a key factor determining resource efficiency in agriculture. The results suggest that applying farming practices, which favour a rich and abundant soil life (e.g. reduced tillage, organic farming, crop rotation), can reduce environmental impacts, enhance crop yield and result in a more sustainable agricultural system. However, this needs to be confirmed in field situations. Enhanced nutrient-use efficiency obtained through farming practices which exert positive effects on soil biota could result in reduced amounts of fertilisers needed for agricultural production and reduced nutrient losses to the environment, providing benefits of such practices beyond positive effects on biodiversity.

Community analyses of arbuscular mycorrhizal fungi (AMF) using ribosomal small subunit (SSU) or internal transcribed spacer (ITS) DNA sequences often suffer from low resolution or coverage. We developed a novel sequencing based approach for a highly resolving and specific profiling of AMF communities. We took advantage of previously established AMF-specific PCR primers that amplify a c. 1.5-kb long fragment covering parts of SSU, ITS and parts of the large ribosomal subunit (LSU), and we sequenced the resulting amplicons with single molecule real-time (SMRT) sequencing. The method was applicable to soil and root samples, detected all major AMF families and successfully discriminated closely related AMF species, which would not be discernible using SSU sequences. In inoculation tests we could trace the introduced AMF inoculum at the molecular level. One of the introduced strains almost replaced the local strain(s), revealing that AMF inoculation can have a profound impact on the native community. The methodology presented offers researchers a powerful new tool for AMF community analysis because it unifies improved specificity and enhanced resolution, whereas the drawback of medium sequencing throughput appears of lesser importance for low-diversity groups such as AMF.

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Plant roots are major transmitters of atmospheric carbon into soil. The rhizosphere, the soil volume around living roots influenced by root activities, represents hotspots for organic carbon (OC) inputs, microbial activity, and carbon turnover. Rhizosphere processes remain poorly understood and the observation of key mechanisms for carbon transfer and protection in intact rhizosphere microenvironments are challenging. We deciphered the fate of photosynthesis-derived OC in intact wheat rhizosphere, combining stable isotope labeling at field scale with high-resolution 3D-imaging. We used nano-scale secondary ion mass spectrometry and focus ion beam-scanning electron microscopy to generate insights into rhizosphere processes at nanometer scale. In immature wheat roots, the carbon circulated through the apoplastic pathway, via cell walls, from the stele to the cortex. The carbon was transferred to substantial microbial communuties, mainly represented by bacteria surrounding peripheral root cells. Iron oxides formed bridges between roots and bigger mineral particles, such as quartz, and surrounded bacteria in microaggregates close to the root surface. Some microaggregates were also intimately associated with the fungal hyphae surface. Based on these results, we propose a conceptual model depicting the fate of carbon at biogeochemical interfaces in the rhizosphere, at the forefront of growing roots. We observed complex interplays between vectors (roots, fungi, bacteria), transferring plant-derived OC into root-free soil and stabilizing agents (iron oxides, root and microorganism products), potentially protecting plant-derived OC within microaggregates in the rhizosphere.