Drought effects on trait space of winter wheat are independent of land management.

Investigating plant responses to climate change is key to develop suitable adaptation strategies. However, whether changes in land management can alleviate increasing drought threats to crops in the future is still unclear. We conducted a management × drought experiment with winter wheat (Triticum aestivum L.) to study plant water and vegetative traits in response to drought and management (conventional vs organic farming, with intensive vs conservation tillage). Water traits (root water uptake pattern, stem metaxylem area, leaf water potential, stomatal conductance) and vegetative traits (plant height, leaf area, leaf Chl content) were considered simultaneously to characterise the variability of multiple traits in a trait space, using principal component analysis. Management could not alleviate the drought impacts on plant water traits as it mainly affected vegetative traits, with yields ultimately being affected by both management and drought. Trait spaces were clearly separated between organic and conventional management as well as between drought and control conditions. Moreover, changes in trait space triggered by management and drought were independent from each other. Neither organic management nor conservation tillage eased drought impacts on winter wheat. Thus, our study raised concerns about the effectiveness of these management options as adaptation strategies to climate change.

Land conversion to agriculture induces taxonomic homogenization of soil microbial communities globally.

Agriculture contributes to a decline in local species diversity and to above- and below-ground biotic homogenization. Here, we conduct a continental survey using 1185 soil samples and compare microbial communities from natural ecosystems (forest, grassland, and wetland) with converted agricultural land. We combine our continental survey results with a global meta-analysis of available sequencing data that cover more than 2400 samples across six continents. Our combined results demonstrate that land conversion to agricultural land results in taxonomic and functional homogenization of soil bacteria, mainly driven by the increase in the geographic ranges of taxa in croplands. We find that 20% of phylotypes are decreased and 23% are increased by land conversion, with croplands enriched in Chloroflexi, Gemmatimonadota, Planctomycetota, Myxcoccota and Latescibacterota. Although there is no significant difference in functional composition between natural ecosystems and agricultural land, functional genes involved in nitrogen fixation, phosphorus mineralization and transportation are depleted in cropland. Our results provide a global insight into the consequences of land-use change on soil microbial taxonomic and functional diversity.

The mycorrhizal symbiosis: research frontiers in genomics, ecology, and agricultural application.

Mycorrhizal symbioses between plants and fungi are vital for the soil structure, nutrient cycling, plant diversity, and ecosystem sustainability. More than 250 000 plant species are associated with mycorrhizal fungi. Recent advances in genomics and related approaches have revolutionized our understanding of the biology and ecology of mycorrhizal associations. The genomes of 250+ mycorrhizal fungi have been released and hundreds of genes that play pivotal roles in regulating symbiosis development and metabolism have been characterized. rDNA metabarcoding and metatranscriptomics provide novel insights into the ecological cues driving mycorrhizal communities and functions expressed by these associations, linking genes to ecological traits such as nutrient acquisition and soil organic matter decomposition. Here, we review genomic studies that have revealed genes involved in nutrient uptake and symbiosis development, and discuss adaptations that are fundamental to the evolution of mycorrhizal lifestyles. We also evaluated the ecosystem services provided by mycorrhizal networks and discuss how mycorrhizal symbioses hold promise for sustainable agriculture and forestry by enhancing nutrient acquisition and stress tolerance. Overall, unraveling the intricate dynamics of mycorrhizal symbioses is paramount for promoting ecological sustainability and addressing current pressing environmental concerns. This review ends with major frontiers for further research.

AMF-SporeChip provides new insights into arbuscular mycorrhizal fungal asymbiotic hyphal growth dynamics at the cellular level.

Arbuscular mycorrhizal fungi (AMF) form symbiotic associations with the majority of land plants and deliver a wide range of soil-based ecosystem services. Due to their conspicuous belowground lifestyle in a dark environment surrounded by soil particles, much is still to be learned about the influence of environmental (i.e., physical) cues on spore germination, hyphal morphogenesis and anastomosis/hyphal healing mechanisms. To fill existing gaps in AMF knowledge, we developed a new microfluidic platform - the AMF-SporeChip - to visualise the foraging behaviour of germinating Rhizophagus and Gigaspora spores and confront asymbiotic hyphae with physical obstacles. In combination with timelapse microscopy, the fungi could be examined at the cellular level and in real-time. The AMF-SporeChip allowed us to acquire movies with unprecedented visual clarity and therefore identify various exploration strategies of AMF asymbiotic hyphae. We witnessed tip-to-tip and tip-to-side hyphal anastomosis formation. Anastomosis involved directed hyphal growth in a "stop-and-go" manner, yielding visual evidence of pre-anastomosis signalling and decision-making. Remarkably, we also revealed a so-far undescribed reversible cytoplasmic retraction, including the formation of up to 8 septa upon retraction, as part of a highly dynamic space navigation, probably evolved to optimise foraging efficiency. Our findings demonstrated how AMF employ an intricate mechanism of space searching, involving reversible cytoplasmic retraction, branching and directional changes. In turn, the AMF-SporeChip is expected to open many future frontiers for AMF research.

Biotic homogenization, lower soil fungal diversity and fewer rare taxa in arable soils across Europe.

Soil fungi are a key constituent of global biodiversity and play a pivotal role in agroecosystems. How arable farming affects soil fungal biogeography and whether it has a disproportional impact on rare taxa is poorly understood. Here, we used the high-resolution PacBio Sequel targeting the entire ITS region to investigate the distribution of soil fungi in 217 sites across a 3000 km gradient in Europe. We found a consistently lower diversity of fungi in arable lands than grasslands, with geographic locations significantly impacting fungal community structures. Prevalent fungal groups became even more abundant, whereas rare groups became fewer or absent in arable lands, suggesting a biotic homogenization due to arable farming. The rare fungal groups were narrowly distributed and more common in grasslands. Our findings suggest that rare soil fungi are disproportionally affected by arable farming, and sustainable farming practices should protect rare taxa and the ecosystem services they support.

Interaction effects of pH and land cover on soil microbial diversity are climate-dependent.

Factors regulating the diversity and composition of soil microbial communities include soil properties, land cover and climate. How these factors interact at large scale remains poorly investigated. Here, we used an extensive dataset including 715 locations from 24 European countries to investigate the interactive effects of climatic region, land cover and pH on soil bacteria and fungi. We found that differences in microbial diversity and community composition between land cover types depended on the climatic region. In Atlantic, Boreal and Continental regions, microbial richness was higher in croplands and grasslands than woodlands while richness in Mediterranean areas did not vary significantly among land cover types. These differences were further related to soil pH, as a driver of bacterial and fungal richness in most climatic regions, but the interaction of pH with land cover depended on the region. Microbial community composition differed the most between croplands and woodlands in all regions, mainly due to differences in pH. In the Mediterranean region, bacterial communities in woodlands and grasslands were the most similar, whereas in other regions, grassland and cropland-associated bacteria showed more similarity. Overall, we showed that key factors interact in shaping soil microbial communities in a climate-dependent way at large scale.

A tripartite bacterial-fungal-plant symbiosis in the mycorrhiza-shaped microbiome drives plant growth and mycorrhization.

BACKGROUND: Plant microbiomes play crucial roles in nutrient cycling and plant growth, and are shaped by a complex interplay between plants, microbes, and the environment. The role of bacteria as mediators of the 400-million-year-old partnership between the majority of land plants and, arbuscular mycorrhizal (AM) fungi is still poorly understood. Here, we test whether AM hyphae-associated bacteria influence the success of the AM symbiosis. RESULTS: Using partitioned microcosms containing field soil, we discovered that AM hyphae and roots selectively assemble their own microbiome from the surrounding soil. In two independent experiments, we identified several bacterial genera, including Devosia, that are consistently enriched on AM hyphae. Subsequently, we isolated 144 pure bacterial isolates from a mycorrhiza-rich sample of extraradical hyphae and isolated Devosia sp. ZB163 as root and hyphal colonizer. We show that this AM-associated bacterium synergistically acts with mycorrhiza on the plant root to strongly promote plant growth, nitrogen uptake, and mycorrhization. CONCLUSIONS: Our results highlight that AM fungi do not function in  isolation and that the plant-mycorrhiza symbiont can recruit beneficial bacteria that support the symbiosis. Video Abstract.

The microbial contribution to litter decomposition and plant growth.

Soil and plant roots are colonized by highly complex and diverse communities of microbes. It has been proposed that bacteria and fungi have synergistic effects on litter decomposition, but experimental evidence supporting this claim is weak. In this study, we manipulated the composition of two microbial kingdoms (Bacteria and Fungi) in experimental microcosms. In microcosms that were inoculated with fungi, litter loss was 47% higher than in microcosms that were not inoculated or only inoculated with bacteria. Combined inoculation with both bacteria and fungi did not significantly enhance decomposition compared with the fungi-only treatments, and, as such, we found no evidence for complementary effects using our experimental setup. Inoculation with fungi also had a positive impact on plant growth after 4 and 8 weeks (480% and 710% growth stimulation, respectively). After 16 weeks, plant biomass was highest in microcosms where both bacteria and fungi were present pointing to fungal-bacterial complementarity in stimulating plant growth. Overall, this study suggests that fungi are the main decomposers of plant litter and that the inoculated fungi contribute to plant growth in our experimental system.

Pesticides in Agricultural Soils: Major Findings from Various Monitoring Campaigns in Switzerland.

Synthetic pesticides are widely applied in modern agriculture, where they are used against diseases, pests, and weeds to secure crop yield and quality. However, their intensive application has led to widespread contamination of the environment, including soils. Due to their inherent toxicity, they might pose a risk to soil health by causing harm to non-target organisms and disrupting ecosystem services in both agricultural and other exposed soils. Following the Swiss National Action Plan on the reduction of pesticide risks, Agroscope has conducted several soil monitoring studies that are briefly presented here. All of them resort to different multi-residue trace analytical approaches to simultaneously quantify up to about 150 modern pesticides by either accelerated solvent, or Quick, Easy, Cheap, Efficient, Rugged, Safe (QuEChERS) extraction, followed by separation and detection with liquid chromatography-triple quadrupole mass spectrometry. While partly still in progress, our investigations led to the following major findings this far: Multiple pesticides are commonly present in soils, with individual concentrations in agricultural soils often reaching up to a few tens of µg/kg. Pesticide occurrence and concentrations in agricultural soils primarily depend on land use, land use history and cultivated crops. Pesticides can prevail much longer than predicted by their half-lives, and were found in soils even decades after conversion from conventional to organic farming. Corresponding residual fractions can be in the order of a few percent of the originally applied amounts. We further found negative associations of pesticide residues with the abundance of beneficial soil life, underpinning their potential risk to the fertility of agricultural soils. Traces of pesticides are also detected in soils to which they were never applied, indicating contamination, e.g., via spray drift or atmospheric deposition. These results confirm the general notion of both scientists and legislators that prospective risk assessments (RA; as executed during registration and use authorization) should be confirmed and adjusted by retrospective RA (e.g., by environmental monitoring studies of currently used compounds) to jointly lead to an overall reduced environmental risk of pesticides.

Belowground carbon transfer across mycorrhizal networks among trees: Facts, not fantasy.

The mycorrhizal symbiosis between fungi and plants is among the oldest, ubiquitous and most important interactions in terrestrial life on Earth. Carbon (C) transfer across a common mycorrhizal network (CMN) was demonstrated over half a century ago in the lab ( Reid & Woods, 1969), and later in the field ( Simard et al., 1997a). Recent years have seen ample progress in this research direction, including evidence for ecological significance of carbon transfer ( Klein et al., 2016). Furthermore, specific cases where the architecture of mycorrhizal networks have been mapped ( Beiler et al., 2015) and CMN-C transfer from mature trees to seedlings has been demonstrated ( Orrego, 2018) have suggested that trees in forests are more connected than once thought ( Simard, 2021). In a recent Perspective, Karst et al. (2023) offered a valuable critical review warning of over-interpretation and positive citation bias in CMN research. It concluded that while there is evidence for C movement among plants, the importance of CMNs remains unclear, as noted by others too ( Henriksson et al., 2023). Here we argue that while some of these claims are justified, factual evidence about belowground C transfer across CMNs is solid and accumulating.

Soil microbiome indicators can predict crop growth response to large-scale inoculation with arbuscular mycorrhizal fungi.

Alternative solutions to mineral fertilizers and pesticides that reduce the environmental impact of agriculture are urgently needed. Arbuscular mycorrhizal fungi (AMF) can enhance plant nutrient uptake and reduce plant stress; yet, large-scale field inoculation trials with AMF are missing, and so far, results remain unpredictable. We conducted on-farm experiments in 54 fields in Switzerland and quantified the effects on maize growth. Growth response to AMF inoculation was highly variable, ranging from -12% to +40%. With few soil parameters and mainly soil microbiome indicators, we could successfully predict 86% of the variation in plant growth response to inoculation. The abundance of pathogenic fungi, rather than nutrient availability, best predicted (33%) AMF inoculation success. Our results indicate that soil microbiome indicators offer a sustainable biotechnological perspective to predict inoculation success at the beginning of the growing season. This predictability increases the profitability of microbiome engineering as a tool for sustainable agricultural management.

Microbial dynamics in soils of the Damma glacier forefield show succession in the functional genetic potential.

Glacier retreat is a visible consequence of climate change worldwide. Although taxonomic change of the soil microbiomes in glacier forefields have been widely documented, how microbial genetic potential changes along succession is little known. Here, we used shotgun metagenomics to analyse whether the soil microbial genetic potential differed between four stages of soil development (SSD) sampled along three transects in the Damma glacier forefield (Switzerland). The SSDs were characterized by an increasing vegetation cover, from barren soil, to biological soil crust, to sparsely vegetated soil and finally to vegetated soil. Results suggested that SSD significantly influenced microbial genetic potential, with the lowest functional diversity surprisingly occurring in the vegetated soils. Overall, carbohydrate metabolism and secondary metabolite biosynthesis genes overrepresented in vegetated soils, which could be partly attributed to plant-soil feedbacks. For C degradation, glycoside hydrolase genes enriched in vegetated soils, while auxiliary activity and carbohydrate esterases genes overrepresented in barren soils, suggested high labile C degradation potential in vegetated, and high recalcitrant C degradation potential in barren soils. For N-cycling, organic N degradation and synthesis genes dominated along succession, and gene families involved in nitrification were overrepresented in barren soils. Our study provides new insights into how the microbial genetic potential changes during soil formation along the Damma glacier forefield.

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.

Patterns in soil microbial diversity across Europe.

Factors driving microbial community composition and diversity are well established but the relationship with microbial functioning is poorly understood, especially at large scales. We analysed microbial biodiversity metrics and distribution of potential functional groups along a gradient of increasing land-use perturbation, detecting over 79,000 bacterial and 25,000 fungal OTUs in 715 sites across 24 European countries. We found the lowest bacterial and fungal diversity in less-disturbed environments (woodlands) compared to grasslands and highly-disturbed environments (croplands). Highly-disturbed environments contain significantly more bacterial chemoheterotrophs, harbour a higher proportion of fungal plant pathogens and saprotrophs, and have less beneficial fungal plant symbionts compared to woodlands and extensively-managed grasslands. Spatial patterns of microbial communities and predicted functions are best explained when interactions among the major determinants (vegetation cover, climate, soil properties) are considered. We propose guidelines for environmental policy actions and argue that taxonomical and functional diversity should be considered simultaneously for monitoring purposes.

Increasing the number of stressors reduces soil ecosystem services worldwide.

Increasing the number of environmental stressors could decrease ecosystem functioning in soils. Yet this relationship has never been globally assessed outside laboratory experiments. Here, using two independent global standardized field surveys, and a range of natural and human factors, we test the relationship between the number of environmental stressors exceeding different critical thresholds and the maintenance of multiple ecosystem services across biomes. Our analysis shows that, multiple stressors, from medium levels (>50%), negatively and significantly correlates with impacts on ecosystem services, and that multiple stressors crossing a high-level critical threshold (over 75% of maximum observed levels), reduces soil biodiversity and functioning globally. The number of environmental stressors >75% threshold was consistently seen as an important predictor of multiple ecosystem services, therefore improving prediction of ecosystem functioning. Our findings highlight the need to reduce the dimensionality of the human footprint on ecosystems to conserve biodiversity and function.