Soil microbiota as game-changers in restoration of degraded lands.

Land degradation reduces soil functioning and, consequently, the services that soil provides. Soil hydrological functions are critical to combat soil degradation and promote soil restoration. Soil microorganisms affect soil hydrology, but the role of soil microbiota in forming and sustaining soil is not well explored. Case studies indicate the potential of soil microorganisms as game-changers in restoring soil functions. We review the state of the art of microorganism use in land restoration technology, the groups of microorganisms with the greatest potential for soil restoration, knowledge of the effect of microorganisms on soil physical properties, and proposed strategies for the long-term restoration of degraded lands. We also emphasize the need to advance the emerging research field of biophysical landscape interactions to support soil-plant ecosystem restoration practices.

The role of soils in habitat creation, maintenance and restoration.

Soils are the fundament of terrestrial ecosystems. Across the globe we find different soil types with different properties resulting from the interacting soil forming factors: parent material, climate, topography, organisms and time. Here we present the role of soils in habitat formation and maintenance in natural systems, and reflect on how humans have modified soils from local to global scale. Soils host a tremendous diversity of life forms, most of them microscopic in size. We do not yet know all the functionalities of this diversity at the level of individual taxa or through their interactions. However, we do know that the interactions and feedbacks between soil life, plants and soil chemistry and physics are essential for soil and habitat formation, maintenance and restoration. Moreover, the couplings between soils and major cycles of carbon, nutrients and water are essential for supporting the production of food, feed and fibre, drinking water and greenhouse gas balances. Soils take thousands of years to form, yet are lost very quickly through a multitude of stressors. The current status of our soils globally is worrisome, yet with concerted action we can bend the curve and create win-wins of soil and habitat conservation, regeneration and sustainable development. This article is part of the theme issue 'The role of soils in delivering Nature's Contributions to People'.

Soil-derived Nature's Contributions to People and their contribution to the UN Sustainable Development Goals.

This special issue provides an assessment of the contribution of soils to Nature's Contributions to People (NCP). Here, we combine this assessment and previously published relationships between NCP and delivery on the UN Sustainable Development Goals (SDGs) to infer contributions of soils to the SDGs. We show that in addition to contributing positively to the delivery of all NCP, soils also have a role in underpinning all SDGs. While highlighting the great potential of soils to contribute to sustainable development, it is recognized that poorly managed, degraded or polluted soils may contribute negatively to both NCP and SDGs. The positive contribution, however, cannot be taken for granted, and soils must be managed carefully to keep them healthy and capable of playing this vital role. A priority for soil management must include: (i) for healthy soils in natural ecosystems, protect them from conversion and degradation; (ii) for managed soils, manage in a way to protect and enhance soil biodiversity, health and sustainability and to prevent degradation; and (iii) for degraded soils, restore to full soil health. We have enough knowledge now to move forward with the implementation of best management practices to maintain and improve soil health. This analysis shows that this is not just desirable, it is essential if we are to meet the SDG targets by 2030 and achieve sustainable development more broadly in the decades to come. This article is part of the theme issue 'The role of soils in delivering Nature's Contributions to People'.

Leachates from plants recently infected by root-feeding nematodes cause increased biomass allocation to roots in neighbouring plants.

Plants can adjust defence strategies in response to signals from neighbouring plants attacked by aboveground herbivores. Whether similar responses exist to belowground herbivory remains less studied, particularly regarding the spatiotemporal dynamics of such belowground signalling. We grew the grass Agrostis stolonifera with or without root-feeding nematodes (Meloidogyne minor). Leachates were extracted at different distances from these plants and at different times after inoculation. The leachates were applied to receiver A. stolonifera plants, of which root, shoot, and total biomass, root/shoot ratio, shoot height, shoot branch number, maximum rooting depth and root number were measured 3 weeks after leachate application. Receiver plants allocated significantly more biomass to roots when treated with leachates from nematode-inoculated plants at early infection stages. However, receiver plants' root/shoot ratio was similar when receiving leachates collected at later stages from nematode-infected or control plants. Overall, early-collected leachates reduced growth of receiver plants significantly. Plants recently infected by root-feeding nematodes can thus induce increased root proliferation of neighbouring plants through root-derived compounds. Possible explanations for this response include a better tolerance of anticipated root damage by nematodes or the ability to grow roots away from the nematode-infected soil. Further investigations are still needed to identify the exact mechanisms.

Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs.

The effects of plants on the biosphere, atmosphere and geosphere are key determinants of terrestrial ecosystem functioning. However, despite substantial progress made regarding plant belowground components, we are still only beginning to explore the complex relationships between root traits and functions. Drawing on the literature in plant physiology, ecophysiology, ecology, agronomy and soil science, we reviewed 24 aspects of plant and ecosystem functioning and their relationships with a number of root system traits, including aspects of architecture, physiology, morphology, anatomy, chemistry, biomechanics and biotic interactions. Based on this assessment, we critically evaluated the current strengths and gaps in our knowledge, and identify future research challenges in the field of root ecology. Most importantly, we found that belowground traits with the broadest importance in plant and ecosystem functioning are not those most commonly measured. Also, the estimation of trait relative importance for functioning requires us to consider a more comprehensive range of functionally relevant traits from a diverse range of species, across environments and over time series. We also advocate that establishing causal hierarchical links among root traits will provide a hypothesis-based framework to identify the most parsimonious sets of traits with the strongest links on functions, and to link genotypes to plant and ecosystem functioning.

Can flooding-induced greenhouse gas emissions be mitigated by trait-based plant species choice?

Intensively managed grasslands are large sources of the potent greenhouse gas nitrous oxide (N2O) and important regulators of methane (CH4) consumption and production. The predicted increase in flooding frequency and severity due to climate change could increase N2O emissions and shift grasslands from a net CH4 sink to a source. Therefore, effective management strategies are critical for mitigating greenhouse gas emissions from flood-prone grasslands. We tested how repeated flooding affected the N2O and CH4 emissions from 11 different plant communities (Festuca arundinacea, Lolium perenne, Poa trivialis, and Trifolium repens in monoculture, 2- and 4-species mixtures), using intact soil cores from an 18-month old grassland field experiment in a 4-month greenhouse experiment. To elucidate potential underlying mechanisms, we related plant functional traits to cumulative N2O and CH4 emissions. We hypothesized that traits related with fast nitrogen uptake and growth would lower N2O and CH4 emissions in ambient (non-flooded) conditions, and that traits related to tissue toughness would lower N2O and CH4 emissions in flooded conditions. We found that flooding increased cumulative N2O emissions by 97 fold and cumulative CH4 emissions by 1.6 fold on average. Plant community composition mediated the flood-induced increase in N2O emissions. In flooded conditions, increasing abundance of the grass F. arundinacea was related with lower N2O emissions; whereas increases in abundance of the legume T. repens resulted in higher N2O emissions. In non-flooded conditions, N2O emissions were not clearly mediated by plant traits related with nitrogen uptake or biomass production. In flooded conditions, plant communities with high root carbon to nitrogen ratio were related with lower cumulative N2O emissions, and a lower global warming potential (CO2 equivalent of N2O and CH4). We conclude that plant functional traits related to slower decomposition and nitrogen mineralization could play a significant role in mitigating N2O emissions in flooded grasslands.

Increased arbuscular mycorrhizal fungal colonization reduces yield loss of rice (Oryza sativa L.) under drought.

Drought reduces the availability of soil water and the mobility of nutrients, thereby limiting the growth and productivity of rice. Under drought, arbuscular mycorrhizal fungi (AMF) increase P uptake and sustain rice growth. However, we lack knowledge of how the AMF symbiosis contributes to drought tolerance of rice. In the greenhouse, we investigated mechanisms of AMF symbiosis that confer drought tolerance, such as enhanced nutrient uptake, stomatal conductance, chlorophyll fluorescence, and hormonal balance (abscisic acid (ABA) and indole acetic acid (IAA)). Two greenhouse pot experiments comprised three factors in a full factorial design with two AMF treatments (low- and high-AMF colonization), two water treatments (well-watered and drought), and three rice varieties. Soil water potential was maintained at 0 kPa in the well-watered treatment. In the drought treatment, we reduced soil water potential to - 40 kPa in experiment 1 (Expt 1) and to - 80 kPa in experiment 2 (Expt 2). Drought reduced shoot and root dry biomass and grain yield of rice in both experiments. The reduction of grain yield was less with higher AMF colonization. Plants with higher AMF colonization showed higher leaf P concentrations than plants with lower colonization in Expt 1, but not in Expt 2. Plants with higher AMF colonization exhibited higher stomatal conductance and chlorophyll fluorescence than plants with lower colonization, especially under drought. Drought increased the levels of ABA and IAA, and AMF colonization also resulted in higher levels of IAA. The results suggest both nutrient-driven and plant hormone-driven pathways through which AMF confer drought tolerance to rice.

Biodiversity increases multitrophic energy use efficiency, flow and storage in grasslands.

The continuing loss of global biodiversity has raised questions about the risk that species extinctions pose for the functioning of natural ecosystems and the services that they provide for human wellbeing. There is consensus that, on single trophic levels, biodiversity sustains functions; however, to understand the full range of biodiversity effects, a holistic and multitrophic perspective is needed. Here, we apply methods from ecosystem ecology that quantify the structure and dynamics of the trophic network using ecosystem energetics to data from a large grassland biodiversity experiment. We show that higher plant diversity leads to more energy stored, greater energy flow and higher community-energy-use efficiency across the entire trophic network. These effects of biodiversity on energy dynamics were not restricted to only plants but were also expressed by other trophic groups and, to a similar degree, in aboveground and belowground parts of the ecosystem, even though plants are by far the dominating group in the system. The positive effects of biodiversity on one trophic level were not counteracted by the negative effects on adjacent levels. Trophic levels jointly increased the performance of the community, indicating ecosystem-wide multitrophic complementarity, which is potentially an important prerequisite for the provisioning of ecosystem services.

Soil fauna diversity increases CO2 but suppresses N2 O emissions from soil.

Soil faunal activity can be a major control of greenhouse gas (GHG) emissions from soil. Effects of single faunal species, genera or families have been investigated, but it is unknown how soil fauna diversity may influence emissions of both carbon dioxide (CO2 , end product of decomposition of organic matter) and nitrous oxide (N2 O, an intermediate product of N transformation processes, in particular denitrification). Here, we studied how CO2 and N2 O emissions are affected by species and species mixtures of up to eight species of detritivorous/fungivorous soil fauna from four different taxonomic groups (earthworms, potworms, mites, springtails) using a microcosm set-up. We found that higher species richness and increased functional dissimilarity of species mixtures led to increased faunal-induced CO2 emission (up to 10%), but decreased N2 O emission (up to 62%). Large ecosystem engineers such as earthworms were key drivers of both CO2 and N2 O emissions. Interestingly, increased biodiversity of other soil fauna in the presence of earthworms decreased faunal-induced N2 O emission despite enhanced C cycling. We conclude that higher soil fauna functional diversity enhanced the intensity of belowground processes, leading to more complete litter decomposition and increased CO2 emission, but concurrently also resulting in more complete denitrification and reduced N2 O emission. Our results suggest that increased soil fauna species diversity has the potential to mitigate emissions of N2 O from soil ecosystems. Given the loss of soil biodiversity in managed soils, our findings call for adoption of management practices that enhance soil biodiversity and stimulate a functionally diverse faunal community to reduce N2 O emissions from managed soils.

Feedbacks of plant identity and diversity on the diversity and community composition of rhizosphere microbiomes from a long-term biodiversity experiment.

Soil microbes are known to be key drivers of several essential ecosystem processes such as nutrient cycling, plant productivity and the maintenance of plant species diversity. However, how plant species diversity and identity affect soil microbial diversity and community composition in the rhizosphere is largely unknown. We tested whether, over the course of 11 years, distinct soil bacterial communities developed under plant monocultures and mixtures, and if over this time frame plants with a monoculture or mixture history changed in the bacterial communities they associated with. For eight species, we grew offspring of plants that had been grown for 11 years in the same field monocultures or mixtures (plant history in monoculture vs. mixture) in pots inoculated with microbes extracted from the field monoculture and mixture soils attached to the roots of the host plants (soil legacy). After 5 months of growth in the glasshouse, we collected rhizosphere soil from each plant and used 16S rRNA gene sequencing to determine the community composition and diversity of the bacterial communities. Bacterial community structure in the plant rhizosphere was primarily determined by soil legacy and by plant species identity, but not by plant history. In seven of the eight plant species the number of individual operational taxonomic units with increased abundance was larger when inoculated with microbes from mixture soil. We conclude that plant species richness can affect below-ground community composition and diversity, feeding back to the assemblage of rhizosphere bacterial communities in newly establishing plants via the legacy in soil.

The Future of Complementarity: Disentangling Causes from Consequences.

Evidence suggests that biodiversity supports ecosystem functioning. Yet, the mechanisms driving this relationship remain unclear. Complementarity is one common explanation for these positive biodiversity-ecosystem functioning relationships. Yet, complementarity is often indirectly quantified as overperformance in mixture relative to monoculture (e.g., 'complementarity effect'). This overperformance is then attributed to the intuitive idea of complementarity or, more specifically, to species resource partitioning. Locally, however, several unassociated causes may drive this overperformance. Here, we differentiate complementarity into three types of species differences that may cause enhanced ecosystem functioning in more diverse ecosystems: (i) resource partitioning, (ii) abiotic facilitation, and (iii) biotic feedbacks. We argue that disentangling these three causes is crucial for predicting the response of ecosystems to future biodiversity loss.

Plant-Soil Feedback: Bridging Natural and Agricultural Sciences.

In agricultural and natural systems researchers have demonstrated large effects of plant-soil feedback (PSF) on plant growth. However, the concepts and approaches used in these two types of systems have developed, for the most part, independently. Here, we present a conceptual framework that integrates knowledge and approaches from these two contrasting systems. We use this integrated framework to demonstrate (i) how knowledge from complex natural systems can be used to increase agricultural resource-use efficiency and productivity and (ii) how research in agricultural systems can be used to test hypotheses and approaches developed in natural systems. Using this framework, we discuss avenues for new research toward an ecologically sustainable and climate-smart future.

What plant functional traits can reduce nitrous oxide emissions from intensively managed grasslands?

Plant species exert a dominant control over the nitrogen (N) cycle of natural and managed grasslands. Although in intensively managed systems that receive large external N inputs the emission of the potent greenhouse gas nitrous oxide (N2 O) is a crucial component of this cycle, a mechanistic relationship between plant species and N2 O emissions has not yet been established. Here we use a plant functional trait approach to study the relation between plant species strategies and N2 O emissions from soils. Compared to species with conservative strategies, species with acquisitive strategies have higher N uptake when there is ample N in the soil, but also trigger N mineralization when soil N is limiting. Therefore, we hypothesized that (1) compared to conservative species, species with acquisitive traits reduce N2 O emissions after a high N addition; and (2) species with conservative traits have lower N2 O emissions than acquisitive plants if there is no high N addition. This was tested in a greenhouse experiment using monocultures of six grass species with differing above- and below-ground traits, growing across a gradient of soil N availability. We found that acquisitive species reduced N2 O emissions at all levels of N availability, produced higher biomass and showed larger N uptake. As such, acquisitive species had 87% lower N2 O emissions per unit of N uptake than conservative species (p < .05). Structural equation modelling revealed that specific leaf area and root length density were key traits regulating the effects of plants on N2 O emission and biomass productivity. These results provide the first framework to understand the mechanisms through which plants modulate N2 O emissions, pointing the way to develop productive grasslands that contribute optimally to climate change mitigation.

Community evolution increases plant productivity at low diversity.

Species extinctions from local communities negatively affect ecosystem functioning. Ecological mechanisms underlying these impacts are well studied, but the role of evolutionary processes is rarely assessed. Using a long-term field experiment, we tested whether natural selection in plant communities increased biodiversity effects on productivity. We re-assembled communities with 8-year co-selection history adjacent to communities with identical species composition but no history of co-selection ('naïve communities'). Monocultures, and in particular mixtures of two to four co-selected species, were more productive than their corresponding naïve communities over 4 years in soils with or without co-selected microbial communities. At the highest diversity level of eight plant species, no such differences were observed. Our findings suggest that plant community evolution can lead to rapid increases in ecosystem functioning at low diversity but may take longer at high diversity. This effect was not modified by treatments simulating co-evolutionary processes between plants and soil organisms.

Spatial heterogeneity in root litter and soil legacies differentially affect legume root traits.

BACKGROUND AND AIMS: Plants affect the soil environment via litter inputs and changes in biotic communities, which feed back to subsequent plant growth. Here we investigated the individual contributions of litter and biotic communities to soil feedback effects, and plant ability to respond to spatial heterogeneity in soil legacy. METHODS: We tested for localised and systemic responses of Trifolium repens to soil biotic and root litter legacy of seven grassland species by exposing half of a root system to control soil and the other half to specific inoculum or root litter. RESULTS: Soil inoculation triggered a localised reduction in root length while litter locally increased root biomass independent of inoculum or litter species identity. Nodule formation was locally suppressed in response to soil conditioned by another legume (Vicia cracca) and showed a trend towards systemic reduction in response to conspecific soil. V. cracca litter also caused a systemic response with thinner roots produced in the part of the root system not directly exposed to the litter. CONCLUSIONS: Spatial heterogeneity in root litter distribution and soil communities generate distinct local and systemic responses in root morphology and nodulation. These responses can influence plant-mutualist interactions and nutrient cycling, and should be included in plant co-existence models.

Symbiotic soil fungi enhance ecosystem resilience to climate change.

Substantial amounts of nutrients are lost from soils through leaching. These losses can be environmentally damaging, causing groundwater eutrophication and also comprise an economic burden in terms of lost agricultural production. More intense precipitation events caused by climate change will likely aggravate this problem. So far it is unresolved to which extent soil biota can make ecosystems more resilient to climate change and reduce nutrient leaching losses when rainfall intensity increases. In this study, we focused on arbuscular mycorrhizal (AM) fungi, common soil fungi that form symbiotic associations with most land plants and which increase plant nutrient uptake. We hypothesized that AM fungi mitigate nutrient losses following intensive precipitation events (higher amount of precipitation and rain events frequency). To test this, we manipulated the presence of AM fungi in model grassland communities subjected to two rainfall scenarios: moderate and high rainfall intensity. The total amount of nutrients lost through leaching increased substantially with higher rainfall intensity. The presence of AM fungi reduced phosphorus losses by 50% under both rainfall scenarios and nitrogen losses by 40% under high rainfall intensity. Thus, the presence of AM fungi enhanced the nutrient interception ability of soils, and AM fungi reduced the nutrient leaching risk when rainfall intensity increases. These findings are especially relevant in areas with high rainfall intensity (e.g., such as the tropics) and for ecosystems that will experience increased rainfall due to climate change. Overall, this work demonstrates that soil biota such as AM fungi can enhance ecosystem resilience and reduce the negative impact of increased precipitation on nutrient losses.

Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity.

Plants are known to influence belowground microbial community structure along their roots, but the impacts of plant species richness and plant functional group (FG) identity on microbial communities in the bulk soil are still not well understood. Here, we used 454-pyrosequencing to analyse the soil microbial community composition in a long-term biodiversity experiment at Jena, Germany. We examined responses of bacteria, fungi, archaea, and protists to plant species richness (communities varying from 1 to 60 sown species) and plant FG identity (grasses, legumes, small herbs, tall herbs) in bulk soil. We hypothesized that plant species richness and FG identity would alter microbial community composition and have a positive impact on microbial species richness. Plant species richness had a marginal positive effect on the richness of fungi, but we observed no such effect on bacteria, archaea and protists. Plant species richness also did not have a large impact on microbial community composition. Rather, abiotic soil properties partially explained the community composition of bacteria, fungi, arbuscular mycorrhizal fungi (AMF), archaea and protists. Plant FG richness did not impact microbial community composition; however, plant FG identity was more effective. Bacterial richness was highest in legume plots and lowest in small herb plots, and AMF and archaeal community composition in legume plant communities was distinct from that in communities composed of other plant FGs. We conclude that soil microbial community composition in bulk soil is influenced more by changes in plant FG composition and abiotic soil properties, than by changes in plant species richness per se.

Plant diversity and root traits benefit physical properties key to soil function in grasslands.

Plant diversity loss impairs ecosystem functioning, including important effects on soil. Most studies that have explored plant diversity effects belowground, however, have largely focused on biological processes. As such, our understanding of how plant diversity impacts the soil physical environment remains limited, despite the fundamental role soil physical structure plays in ensuring soil function and ecosystem service provision. Here, in both a glasshouse and a long-term field study, we show that high plant diversity in grassland systems increases soil aggregate stability, a vital structural property of soil, and that root traits play a major role in determining diversity effects. We also reveal that the presence of particular plant species within mixed communities affects an even wider range of soil physical processes, including hydrology and soil strength regimes. Our results indicate that alongside well-documented effects on ecosystem functioning, plant diversity and root traits also benefit essential soil physical properties.

Plant selection and soil legacy enhance long-term biodiversity effects.

Plant-plant and plant-soil interactions can help maintain plant diversity and ecosystem functions. Changes in these interactions may underlie experimentally observed increases in biodiversity effects over time via the selection of genotypes adapted to low or high plant diversity. Little is known, however, about such community-history effects and particularly the role of plant-soil interactions in this process. Soil-legacy effects may occur if co-evolved interactions with soil communities either positively or negatively modify plant biodiversity effects. We tested how plant selection and soil legacy influence biodiversity effects on productivity, and whether such effects increase the resistance of the communities to invasion by weeds. We used two plant selection treatments: parental plants growing in monoculture or in mixture over 8 yr in a grassland biodiversity experiment in the field, which we term monoculture types and mixture types. The two soil-legacy treatments used in this study were neutral soil inoculated with live or sterilized soil inocula collected from the same plots in the biodiversity experiment. For each of the four factorial combinations, seedlings of eight species were grown in monocultures or four-species mixtures in pots in an experimental garden over 15 weeks. Soil legacy (live inoculum) strongly increased biodiversity complementarity effects for communities of mixture types, and to a significantly weaker extent for communities of monoculture types. This may be attributed to negative plant-soil feedbacks suffered by mixture types in monocultures, whereas monoculture types had positive plant-soil feedbacks, in both monocultures and mixtures. Monocultures of mixture types were most strongly invaded by weeds, presumably due to increased pathogen susceptibility, reduced biomass, and altered plant-soil interactions of mixture types. These results show that biodiversity effects in experimental grassland communities can be modified by the evolution of positive vs. negative plant-soil feedbacks of plant monoculture vs. mixture types.

Plant selection and soil legacy enhance long-term biodiversity effects.

Plant-plant and plant-soil interactions can help maintain plant diversity and ecosystem functions. Changes in these interactions may underlie experimentally observed increases in biodiversity effects over time via the selection of genotypes adapted to low or high plant diversity. Little is known, however, about such community-history effects and particularly the role of plant-soil interactions in this process. Soil-legacy effects may occur if co-evolved interactions with soil communities either positively or negatively modify plant biodiversity effects. We tested how plant selection and soil legacy influence biodiversity effects on productivity, and whether such effects increase the resistance of the communities to invasion by weeds. We used two plant selection treatments: parental plants growing in monoculture or in mixture over 8 yr in a grassland biodiversity experiment in the field, which we term monoculture types and mixture types. The two soil-legacy treatments used in this study were neutral soil inoculated with live or sterilized soil inocula collected from the same plots in the biodiversity experiment. For each of the four factorial combinations, seedlings of eight species were grown in monocultures or four-species mixtures in pots in an experimental garden over 15 weeks. Soil legacy (live inoculum) strongly increased biodiversity complementarity effects for communities of mixture types, and to a significantly weaker extent for communities of monoculture types. This may be attributed to negative plant-soil feedbacks suffered by mixture types in monocultures, whereas monoculture types had positive plant-soil feedbacks, in both monocultures and mixtures. Monocultures of mixture types were most strongly invaded by weeds, presumably due to increased pathogen susceptibility, reduced biomass, and altered plant-soil interactions of mixture types. These results show that biodiversity effects in experimental grassland communities can be modified by the evolution of positive vs. negative plant-soil feedbacks of plant monoculture vs. mixture types.