Simplification of soil biota communities impairs nutrient recycling and enhances above- and belowground nitrogen losses.

Agriculture is a major source of nutrient pollution, posing a threat to the earth system functioning. Factors determining the nutrient use efficiency of plant-soil systems need to be identified to develop strategies to reduce nutrient losses while ensuring crop productivity. The potential of soil biota to tighten nutrient cycles by improving plant nutrition and reducing soil nutrient losses is still poorly understood. We manipulated soil biota communities in outdoor lysimeters, planted maize, continuously collected leachates, and measured N2 O- and N2 -gas emissions after a fertilization pulse to test whether differences in soil biota communities affected nutrient recycling and N losses. Lysimeters with strongly simplified soil biota communities showed reduced crop N (-20%) and P (-58%) uptake, strongly increased N leaching losses (+65%), and gaseous emissions (+97%) of N2 O and N2 . Soil metagenomic analyses revealed differences in the abundance of genes responsible for nutrient uptake, nitrate reduction, and denitrification that helped explain the observed nutrient losses. Soil biota are major drivers of nutrient cycling and reductions in the diversity or abundance of certain groups (e.g. through land-use intensification) can disrupt nutrient cycling, reduce agricultural productivity and nutrient use efficiency, and exacerbate environmental pollution and global warming.

Enumerating soil biodiversity.

Soil is an immense habitat for diverse organisms across the tree of life, but just how many organisms live in soil is surprisingly unknown. Previous efforts to enumerate soil biodiversity consider only certain types of organisms (e.g., animals) or report values for diverse groups without partitioning species that live in soil versus other habitats. Here, we reviewed the biodiversity literature to show that soil is likely home to 59 ± 15% of the species on Earth. We therefore estimate an approximately two times greater soil biodiversity than previous estimates, and we include representatives from the simplest (microbial) to most complex (mammals) organisms. Enchytraeidae have the greatest percentage of species in soil (98.6%), followed by fungi (90%), Plantae (85.5%), and Isoptera (84.2%). Our results demonstrate that soil is the most biodiverse singular habitat. By using this estimate of soil biodiversity, we can more accurately and quantitatively advocate for soil organismal conservation and restoration as a central goal of the Anthropocene.

A symbiotic footprint in the plant root microbiome.

BACKGROUND: A major aim in plant microbiome research is determining the drivers of plant-associated microbial communities. While soil characteristics and host plant identity present key drivers of root microbiome composition, it is still unresolved whether the presence or absence of important plant root symbionts also determines overall microbiome composition. Arbuscular mycorrhizal fungi (AMF) and N-fixing rhizobia bacteria are widespread, beneficial root symbionts that significantly enhance plant nutrition, plant health, and root structure. Thus, we hypothesized that symbiont types define the root microbiome structure. RESULTS: We grew 17 plant species from five families differing in their symbiotic associations (no symbioses, AMF only, rhizobia only, or AMF and rhizobia) in a greenhouse and used bacterial and fungal amplicon sequencing to characterize their root microbiomes. Although plant phylogeny and species identity were the most important factors determining root microbiome composition, we discovered that the type of symbioses also presented a significant driver of diversity and community composition. We found consistent responses of bacterial phyla, including members of the Acidobacteria, Chlamydiae, Firmicutes, and Verrucomicrobia, to the presence or absence of AMF and rhizobia and identified communities of OTUs specifically enriched in the different symbiotic groups. A total of 80, 75 and 57 bacterial OTUs were specific for plant species without symbiosis, plant species forming associations with AMF or plant species associating with both AMF and rhizobia, respectively. Similarly, 9, 14 and 4 fungal OTUs were specific for these plant symbiont groups. Importantly, these generic symbiosis footprints in microbial community composition were also apparent in absence of the primary symbionts. CONCLUSION: Our results reveal that symbiotic associations of the host plant leaves an imprint on the wider root microbiome - which we term the symbiotype. These findings suggest the existence of a fundamental assembly principle of root microbiomes, dependent on the symbiotic associations of the host plant.

Arbuscular mycorrhizal fungi mitigate soil nitrogen and phosphorus losses: A meta-analysis.

Nutrient loss from terrestrial ecosystems via leaching and gaseous emissions is increasingly threatening global environmental and human health. Although arbuscular mycorrhizal fungi (AMF) have been shown to regulate soil N and P losses, a comprehensive quantitative overview of their influences on the losses of these soil nutrients across global scales is currently lacking. This study used a meta-analysis of 322 observations from 36 studies to assess the effect of AMF inoculum on 11 variables related to the loss of soil N and P. We found that the presence of AMF significantly reduced soil N and P losses, with the most pronounced reduction occurring in soil NO3--N (-32%), followed by total P (-21%), available P (-16%) and N2O (-10%). However, the mitigation effects of AMF on soil N and P loss were dependent on the identity of AMF inoculum, plant type and soil biotic and abiotic factors. Generally, the mitigation effects of AMF increased with increasing AMF root colonization rate, microbial diversity of inoculants, soil organic carbon (SOC) content and experimental duration as well as with decreasing soil sand contents and soil N and P availability. Overall, this meta-analysis highlights the importance of AMF inoculation in mitigating N and P nutrient loss and environmental pollution for terrestrial ecosystem sustainability.

Enrichment of nosZ-type denitrifiers by arbuscular mycorrhizal fungi mitigates N2 O emissions from soybean stubbles.

Hotspots of N2 O emissions are generated from legume residues during decomposition. Arbuscular mycorrhizal fungi (AMF) from co-cultivated intercropped plants may proliferate into the microsites and interact with soil microbes to reduce N2 O emissions. Yet, the mechanisms by which or how mycorrhizal hyphae affect nitrifiers and denitrifiers in the legume residues remain ambiguous. Here, a split-microcosm experiment was conducted to assess hyphae of Rhizophagus aggregatus from neighbouring maize on overall N2 O emissions from stubbles of nodulated or non-nodulated soybean. Soil microbes from fields intercropped with maize/soybean amended with fertilizer nitrogen (SS-N1) or unamended (SS-N0) were added to the soybean chamber only. AMF hyphae consistently reduced N2 O emissions by 20.8%-61.5%. Generally, AMF hyphae promoted the abundance of N2 O-consuming (nosZ-type) denitrifiers and altered their community composition. The effects were partly associated with increasing MBC and DOC. By contrast, AMF reduced the abundance of nirK-type denitrifiers in the nodulated SS-N0 treatment only and that of AOB in the non-nodulated SS-N1 treatment. Taken together, our results show that AMF reduced N2 O emissions from soybean stubbles, mainly through the promotion of N2 O-consuming denitrifiers. This holds promise for mitigating N2 O emissions by manipulating the efficacious AMF and their associated microbes in cereal/legume intercropping systems.

Organic and conservation agriculture promote ecosystem multifunctionality.

Ecosystems provide multiple services to humans. However, agricultural systems are usually evaluated on their productivity and economic performance, and a systematic and quantitative assessment of the multifunctionality of agroecosystems including environmental services is missing. Using a long-term farming system experiment, we evaluated and compared the agronomic, economic, and ecological performance of the most widespread arable cropping systems in Europe: organic, conservation, and conventional agriculture. We analyzed 43 agroecosystem properties and determined overall agroecosystem multifunctionality. We show that organic and conservation agriculture promoted ecosystem multifunctionality, especially by enhancing regulating and supporting services, including biodiversity preservation, soil and water quality, and climate mitigation. In contrast, conventional cropping showed reduced multifunctionality but delivered highest yield. Organic production resulted in higher economic performance, thanks to higher product prices and additional support payments. Our results demonstrate that different cropping systems provide opposing services, enforcing the productivity-environmental protection dilemma for agroecosystem functioning.

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.

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.

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.

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.

Soil biodiversity and soil community composition determine ecosystem multifunctionality.

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.

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.