S. Franz Bender

Soil biodiversity and soil community composition determine ecosystem multifunctionality

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. Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth’s biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.

An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability

Soil organisms are an integral component of ecosystems, but their activities receive little recognition in agricultural management strategies. Here we synthesize the potential of soil organisms to enhance ecosystem service delivery and demonstrate that soil biodiversity promotes multiple ecosystem functions simultaneously (i.e., ecosystem multifunctionality). We apply the concept of ecological intensification to soils and we develop strategies for targeted exploitation of soil biological traits. We compile promising approaches to enhance agricultural sustainability through the promotion of soil biodiversity and targeted management of soil community composition. We present soil ecological engineering as a concept to generate human land-use systems, which can serve immediate human needs while minimizing environmental impacts.

Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil

N2O 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 N2O emissions from soil. To test for a functional relationship between AMF and N2O 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. N2O 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 N2O 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 N2O emission and altered water relations. Moreover, the abundance of key genes responsible for N2O production (nirK) was negatively and for N2O consumption (nosZ) positively correlated to AMF abundance, indicating that the regulation of N2O 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 N2O emissions.

Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses

Summary 1. 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 (� 51%, corresponding to a reduction of 76 kg N ha � 1 ). 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 (� 25%), defined as g P leached per kg P plant uptake, as well as relative N leaching losses (� 36%), 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 biodiver

The role of arbuscular mycorrhizas in reducing soil nutrient loss

Substantial amounts of nutrients are lost from soils via leaching and as gaseous emissions. These losses can be environmentally damaging and expensive in terms of lost agricultural production. Plants have evolved many traits to optimize nutrient acquisition, including the formation of arbuscular mycorrhizas (AM), associations of plant roots with fungi that acquire soil nutrients. There is emerging evidence that AM have the ability to reduce nutrient loss from soils by enlarging the nutrient interception zone and preventing nutrient loss after rain-induced leaching events. Until recently, this important ecosystem service of AM had been largely overlooked. Here we review the role of AM in reducing nutrient loss and conclude that this role cannot be ignored if we are to increase global food production in an environmentally sustainable manner.

High‐resolution community profiling of arbuscular mycorrhizal fungi

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.

Combined Field Inoculations of Pseudomonas Bacteria, Arbuscular Mycorrhizal Fungi, and Entomopathogenic Nematodes and their Effects on Wheat Performance

In agricultural ecosystems, pest insects, pathogens, and reduced soil fertility pose major challenges to crop productivity and are responsible for significant yield losses worldwide. Management of belowground pests and diseases remains particularly challenging due to the complex nature of the soil and the limited reach of conventional agrochemicals. Boosting the presence of beneficial rhizosphere organisms is a potentially sustainable alternative and may help to optimize crop health and productivity. Field application of single beneficial soil organisms has shown satisfactory results under optimal conditions. This might be further enhanced by combining multiple beneficial soil organisms, but this remains poorly investigated. Here, we inoculated wheat plots with combinations of three beneficial soil organisms that have different rhizosphere functions and studied their effects on crop performance. Plant beneficial Pseudomonas bacteria, arbuscular mycorrhizal fungi (AMF), and entomopathogenic nematodes (EPN), were inoculated individually or in combinations at seeding, and their effects on plant performance were evaluated throughout the season. We used traditional and molecular identification tools to monitor their persistence over the cropping season in augmented and control treatments, and to estimate the possible displacement of native populations. In three separate trials, beneficial soil organisms were successfully introduced into the native populations and readily survived the field conditions. Various Pseudomonas, mycorrhiza, and nematode treatments improved plant health and productivity, while their combinations provided no significant additive or synergistic benefits compared to when applied alone. EPN application temporarily displaced some of the native EPN, but had no significant long-term effect on the associated food web. The strongest positive effect on wheat survival was observed for Pseudomonas and AMF during a season with heavy natural infestation by the frit fly, Oscinella frit, a major pest of cereals. Hence, beneficial impacts differed between the beneficial soil organisms and were most evident for plants under biotic stress. Overall, our findings indicate that in wheat production under the test conditions the three beneficial soil organisms can establish nicely and are compatible, but their combined application provides no additional benefits. Further studies are required, also in other cropping systems, to fine-tune the functional interactions among beneficial soil organisms, crops, and the environment.

Linking 3D Soil Structure and Plant-Microbe-Soil Carbon Transfer in the Rhizosphere

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 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 organic carbon (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.

Strategies for Environmentally Sound Soil Ecological Engineering: A Reply to Machado et al.

Recently, we proposed that soil ecological engineering can be used to enhance agricultural sustainability [1]. In their response to our article, Machado et al. [2] stress the point that potential undesirable side effects of soil ecological manipulations have to be considered and carefully investigated. We fully agree with their general appeal to consider ecological consequences of ecosystem manipulations (see also p. 447 in [1]). However, we want to recall that there are no human activities without a certain impact on ecosystems.