Heritable microbiome variation is correlated with source environment in locally adapted maize varieties.

Beneficial interactions with microorganisms are pivotal for crop performance and resilience. However, it remains unclear how heritable the microbiome is with respect to the host plant genotype and to what extent host genetic mechanisms can modulate plant-microbiota interactions in the face of environmental stresses. Here we surveyed 3,168 root and rhizosphere microbiome samples from 129 accessions of locally adapted Zea, sourced from diverse habitats and grown under control and different stress conditions. We quantified stress treatment and host genotype effects on the microbiome. Plant genotype and source environment were predictive of microbiome abundance. Genome-wide association analysis identified host genetic variants linked to both rhizosphere microbiome abundance and source environment. We identified transposon insertions in a candidate gene linked to both the abundance of a keystone bacterium Massilia in our controlled experiments and total soil nitrogen in the source environment. Isolation and controlled inoculation of Massilia alone can contribute to root development, whole-plant biomass production and adaptation to low nitrogen availability. We conclude that locally adapted maize varieties exert patterns of genetic control on their root and rhizosphere microbiomes that follow variation in their home environments, consistent with a role in tolerance to prevailing stress.

A slow-fast trait continuum at the whole community level in relation to land-use intensification.

Organismal functional strategies form a continuum from slow- to fast-growing organisms, in response to common drivers such as resource availability and disturbance. However, whether there is synchronisation of these strategies at the entire community level is unclear. Here, we combine trait data for >2800 above- and belowground taxa from 14 trophic guilds spanning a disturbance and resource availability gradient in German grasslands. The results indicate that most guilds consistently respond to these drivers through both direct and trophically mediated effects, resulting in a 'slow-fast' axis at the level of the entire community. Using 15 indicators of carbon and nutrient fluxes, biomass production and decomposition, we also show that fast trait communities are associated with faster rates of ecosystem functioning. These findings demonstrate that 'slow' and 'fast' strategies can be manifested at the level of whole communities, opening new avenues of ecosystem-level functional classification.

Vegetation type, not the legacy of warming, modifies the response of microbial functional genes and greenhouse gas fluxes to drought in Oro-Arctic and alpine regions.

Climate warming and summer droughts alter soil microbial activity, affecting greenhouse gas (GHG) emissions in Arctic and alpine regions. However, the long-term effects of warming, and implications for future microbial resilience, are poorly understood. Using one alpine and three Arctic soils subjected to in situ long-term experimental warming, we simulated drought in laboratory incubations to test how microbial functional-gene abundance affects fluxes in three GHGs: carbon dioxide, methane, and nitrous oxide. We found that responses of functional gene abundances to drought and warming are strongly associated with vegetation type and soil carbon. Our sites ranged from a wet, forb dominated, soil carbon-rich systems to a drier, soil carbon-poor alpine site. Resilience of functional gene abundances, and in turn methane and carbon dioxide fluxes, was lower in the wetter, carbon-rich systems. However, we did not detect an effect of drought or warming on nitrous oxide fluxes. All gene-GHG relationships were modified by vegetation type, with stronger effects being observed in wetter, forb-rich soils. These results suggest that impacts of warming and drought on GHG emissions are linked to a complex set of microbial gene abundances and may be habitat-specific.

Fossil-fuel-dependent scenarios could lead to a significant decline of global plant-beneficial bacteria abundance in soils by 2100.

Exploiting the potential benefits of plant-associated microbes represents a sustainable approach to enhancing crop productivity. Plant-beneficial bacteria (PBB) provide multiple benefits to plants. However, the biogeography and community structure remain largely unknown. Here we constructed a PBB database to couple microbial taxonomy with their plant-beneficial traits and analysed the global atlas of potential PBB from 4,245 soil samples. We show that the diversity of PBB peaks in low-latitude regions, following a strong latitudinal diversity gradient. The distribution of potential PBB was primarily governed by environmental filtering, which was mainly determined by local climate. Our projections showed that fossil-fuel-dependent future scenarios would lead to a significant decline of potential PBB by 2100, especially biocontrol agents (-1.03%) and stress resistance bacteria (-0.61%), which may potentially threaten global food production and (agro)ecosystem services.

Root litter decomposition is suppressed in species mixtures and in the presence of living roots.

Plant species diversity and identity can significantly modify litter decomposition, but the underlying mechanisms remain elusive, particularly for root litter. Here, we aimed to disentangle the mechanisms by which plant species diversity alters root litter decomposition. We hypothesised that (1) interactions between species in mixed communities result in litter that decomposes faster than litter produced in monocultures; (2) litter decomposition is accelerated in the presence of living plants, especially when the litter and living plant identities are matched (known as home-field advantage).Monocultures and a mixture of four common grassland species were established to obtain individual litter and a 'natural' root litter mixture. An 'artificial' mixed litter was created using litter from monocultures, mixed in the same proportions as the species composition in the natural litter mixtures based on qPCR measurements. These six root litter types were incubated in four monocultures, a four-species mixture and an unplanted soil.Root decomposition was strongly affected by root litter identity and the presence, but not diversity, of living roots. Mixed-species litter decomposed slower than expected based on the decomposition of single-species litters. In addition, the presence of living roots suppressed decomposition independent of the match between litter and living plant identities. Decomposition was not significantly different between the 'natural' and 'artificial' root litter mixtures, indicating that root-root interactions in species mixtures did not affect root chemical quality. Synthesis. Suppressed decomposition in the presence of living roots indicates that interactions between microbial communities associated with living roots and root litter control root litter decomposition. As we found no support for the importance of home-field advantage or interspecific root interactions in modifying decomposition, suppressed decomposition of mixed-species litter seems to be primarily driven by chemical rather than biotic interactions.

Intensive grassland management disrupts below-ground multi-trophic resource transfer in response to drought.

Modification of soil food webs by land management may alter the response of ecosystem processes to climate extremes, but empirical support is limited and the mechanisms involved remain unclear. Here we quantify how grassland management modifies the transfer of recent photosynthates and soil nitrogen through plants and soil food webs during a post-drought period in a controlled field experiment, using in situ 13C and 15N pulse-labelling in intensively and extensively managed fields. We show that intensive management decrease plant carbon (C) capture and its transfer through components of food webs and soil respiration compared to extensive management. We observe a legacy effect of drought on C transfer pathways mainly in intensively managed grasslands, by increasing plant C assimilation and 13C released as soil CO2 efflux but decreasing its transfer to roots, bacteria and Collembola. Our work provides insight into the interactive effects of grassland management and drought on C transfer pathways, and highlights that capture and rapid transfer of photosynthates through multi-trophic networks are key for maintaining grassland resistance to drought.

Deciphering the role of specialist and generalist plant-microbial interactions as drivers of plant-soil feedback.

Feedback between plants and soil microbial communities can be a powerful driver of vegetation dynamics. Plants elicit changes in the soil microbiome that either promote or suppress conspecifics at the same location, thereby regulating population density-dependence and species co-existence. Such effects are often attributed to the accumulation of host-specific antagonistic or beneficial microbiota in the rhizosphere. However, the identity and host-specificity of the microbial taxa involved are rarely empirically assessed. Here we review the evidence for host-specificity in plant-associated microbes and propose that specific plant-soil feedbacks can also be driven by generalists. We outline the potential mechanisms by which generalist microbial pathogens, mutualists and decomposers can generate differential effects on plant hosts and synthesize existing evidence to predict these effects as a function of plant investments into defence, microbial mutualists and dispersal. Importantly, the capacity of generalist microbiota to drive plant-soil feedbacks depends not only on the traits of individual plants but also on the phylogenetic and functional diversity of plant communities. Identifying factors that promote specialization or generalism in plant-microbial interactions and thereby modulate the impact of microbiota on plant performance will advance our understanding of the mechanisms underlying plant-soil feedback and the ways it contributes to plant co-existence.

Comparing root exudate collection techniques: An improved hybrid method.

1. Plant-microbe interactions are critical for ecosystem functioning and drive rhizosphere processes. Root exudates are an important soil carbon (C) input, as well as a mechanism for communication between plants and rhizosphere microbes, but are notoriously difficult to extract and characterise. Common methods produce either substantial noise from the soil or do not mimic natural systems. Optimising methods for root exudate collection in soil is crucial for advancing our understanding of root-microbe interactions under changing environmental conditions. 2. Hybrid root exudate collection methods, where plants are grown in soil and transferred to hydroponics for exudate collection after root washing, might offer an ecologically relevant alternative to existing approaches. However, this method causes potential root damage as well as osmosis and subsequent leaking of cell contents. Here, we assessed different 'root recovery' periods after root washing and before hybrid root exudate collection, by comparing root exudate quantity and quality with both damaged root extracts and with leachates collected from the intact root-soil system. This was done across three common grassland species representing three functional groups. 3. We found that root exudate profiles of the shortest recovery period (0 days) were similar to damaged root extracts and were very high in C. With an increasing period of root recovery, profiles were more similar to leachates collected from the intact root-soil system, and C concentrations decreased. While both hybrid and leachate collection methods separated species by their root exudate profiles, the hybrid method was less variable in terms of the amount of C measured and provided a more diverse and abundant metabolome with better identification of metabolites. 4. Our results show that a recovery period after root washing of at least 3 days is critical to prevent root damage bias in hybrid collection methods, and that our hybrid method yields exudates that discriminate between species. Our data also suggest that exudates collected with this hybrid method are ecologically valid, which is vital for gaining a mechanistic understanding of their role in ecosystem functioning.

Global data on earthworm abundance, biomass, diversity and corresponding environmental properties.

Earthworms are an important soil taxon as ecosystem engineers, providing a variety of crucial ecosystem functions and services. Little is known about their diversity and distribution at large spatial scales, despite the availability of considerable amounts of local-scale data. Earthworm diversity data, obtained from the primary literature or provided directly by authors, were collated with information on site locations, including coordinates, habitat cover, and soil properties. Datasets were required, at a minimum, to include abundance or biomass of earthworms at a site. Where possible, site-level species lists were included, as well as the abundance and biomass of individual species and ecological groups. This global dataset contains 10,840 sites, with 184 species, from 60 countries and all continents except Antarctica. The data were obtained from 182 published articles, published between 1973 and 2017, and 17 unpublished datasets. Amalgamating data into a single global database will assist researchers in investigating and answering a wide variety of pressing questions, for example, jointly assessing aboveground and belowground biodiversity distributions and drivers of biodiversity change.

Plant Genetic Networks Shaping Phyllosphere Microbial Community.

Phyllosphere microbial communities inhabit the aerial plant parts, such as leaves and flowers, where they form complex molecular interactions with the host plant. Contrary to the relatively well-studied rhizosphere microbiome, scientists are just starting to understand, and potentially utilize, the phyllosphere microbiome. In this article, we summarize the recent studies that have provided novel insights into the mechanism of the host genotype shaping the phyllosphere microbiome and the possibility to select a stable and well-adapted microbiome. We also discuss the most pressing gaps in our knowledge and identify the most promising research directions and tools for understanding the assembly and function of phyllosphere microbiomes - this understanding is necessary if we are to harness phyllosphere microbiomes for improving plant growth and health in managed systems.

Root traits explain rhizosphere fungal community composition among temperate grassland plant species.

While it is known that interactions between plants and soil fungi drive many essential ecosystem functions, considerable uncertainty exists over the drivers of fungal community composition in the rhizosphere. Here, we examined the roles of plant species identity, phylogeny and functional traits in shaping rhizosphere fungal communities and tested the robustness of these relationships to environmental change. We conducted a glasshouse experiment consisting of 21 temperate grassland species grown under three different environmental treatments and characterised the fungal communities within the rhizosphere of these plants. We found that plant species identity, plant phylogenetic relatedness and plant traits all affected rhizosphere fungal community composition. Trait relationships with fungal communities were primarily driven by interactions with arbuscular mycorrhizal fungi, and root traits were stronger predictors of fungal communities than leaf traits. These patterns were independent of the environmental treatments the plants were grown under. Our results showcase the key role of plant root traits, especially root diameter, root nitrogen and specific root length, in driving rhizosphere fungal community composition, demonstrating the potential for root traits to be used within predictive frameworks of plant-fungal relationships. Furthermore, we highlight how key limitations in our understanding of fungal function may obscure previously unmeasured plant-fungal interactions.

Forest fire induces short-term shifts in soil food webs with consequences for carbon cycling.

We tested for fire-induced (5-6 years post-fire) changes in the structure and functioning of the soil food web along a 3000-km north-south transect across European Russia, spanning all major forest types in the northern hemisphere outside the tropics. The total biomass of the detrital food web, including microbes and invertebrates, was not affected by fire. However, fire reduced the biomass of microfauna and mites, but had no impact on mesofauna or macrofauna. Fire also reduced rates of carbon (C) mobilisation by soil biota. Our results demonstrate that fire-induced shifts in soil food webs have significant short-term effects on forest soil C cycling, but that these effects vary across forest types and geographic locations.

Harnessing rhizosphere microbiomes for drought-resilient crop production.

Root-associated microbes can improve plant growth, and they offer the potential to increase crop resilience to future drought. Although our understanding of the complex feedbacks between plant and microbial responses to drought is advancing, most of our knowledge comes from non-crop plants in controlled experiments. We propose that future research efforts should attempt to quantify relationships between plant and microbial traits, explicitly focus on food crops, and include longer-term experiments under field conditions. Overall, we highlight the need for improved mechanistic understanding of the complex feedbacks between plants and microbes during, and particularly after, drought. This requires integrating ecology with plant, microbiome, and molecular approaches and is central to making crop production more resilient to our future climate.

Plant root exudation under drought: implications for ecosystem functioning.

Root exudates are a pathway for plant-microbial communication and play a key role in ecosystem response to environmental change. Here, we collate recent evidence that shows that plants of different growth strategies differ in their root exudation, that root exudates can select for beneficial soil microbial communities, and that drought affects the quantity and quality of root exudation. We use this evidence to argue for a central involvement of root exudates in plant and microbial response to drought and propose a framework for understanding how root exudates influence ecosystem form and function during and after drought. Specifically, we propose that fast-growing plants modify their root exudates to recruit beneficial microbes that facilitate their regrowth after drought, with cascading impacts on their abundance and ecosystem functioning. We identify outstanding questions and methodological challenges that need to be addressed to advance and solidify our comprehension of the importance of root exudates in ecosystem response to drought.

Towards an integrative understanding of soil biodiversity.

Soil is one of the most biodiverse terrestrial habitats. Yet, we lack an integrative conceptual framework for understanding the patterns and mechanisms driving soil biodiversity. One of the underlying reasons for our poor understanding of soil biodiversity patterns relates to whether key biodiversity theories (historically developed for aboveground and aquatic organisms) are applicable to patterns of soil biodiversity. Here, we present a systematic literature review to investigate whether and how key biodiversity theories (species-energy relationship, theory of island biogeography, metacommunity theory, niche theory and neutral theory) can explain observed patterns of soil biodiversity. We then discuss two spatial compartments nested within soil at which biodiversity theories can be applied to acknowledge the scale-dependent nature of soil biodiversity.

Global distribution of earthworm diversity.

Soil organisms, including earthworms, are a key component of terrestrial ecosystems. However, little is known about their diversity, their distribution, and the threats affecting them. We compiled a global dataset of sampled earthworm communities from 6928 sites in 57 countries as a basis for predicting patterns in earthworm diversity, abundance, and biomass. We found that local species richness and abundance typically peaked at higher latitudes, displaying patterns opposite to those observed in aboveground organisms. However, high species dissimilarity across tropical locations may cause diversity across the entirety of the tropics to be higher than elsewhere. Climate variables were found to be more important in shaping earthworm communities than soil properties or habitat cover. These findings suggest that climate change may have serious implications for earthworm communities and for the functions they provide.

Drought decreases incorporation of recent plant photosynthate into soil food webs regardless of their trophic complexity.

Theory suggests that more complex food webs promote stability and can buffer the effects of perturbations, such as drought, on soil organisms and ecosystem functions. Here, we tested experimentally how soil food web trophic complexity modulates the response to drought of soil functions related to carbon cycling and the capture and transfer below-ground of recent photosynthate by plants. We constructed experimental systems comprising soil communities with one, two or three trophic levels (microorganisms, detritivores and predators) and subjected them to drought. We investigated how food web trophic complexity in interaction with drought influenced litter decomposition, soil CO2 efflux, mycorrhizal colonization, fungal production, microbial communities and soil fauna biomass. Plants were pulse-labelled after the drought with 13 C-CO2 to quantify the capture of recent photosynthate and its transfer below-ground. Overall, our results show that drought and soil food web trophic complexity do not interact to affect soil functions and microbial community composition, but act independently, with an overall stronger effect of drought. After drought, the net uptake of 13 C by plants was reduced and its retention in plant biomass was greater, leading to a strong decrease in carbon transfer below-ground. Although food web trophic complexity influenced the biomass of Collembola and fungal hyphal length, 13 C enrichment and the net transfer of carbon from plant shoots to microbes and soil CO2 efflux were not affected significantly by varying the number of trophic groups. Our results indicate that drought has a strong effect on above-ground-below-ground linkages by reducing the flow of recent photosynthate. Our results emphasize the sensitivity of the critical pathway of recent photosynthate transfer from plants to soil organisms to a drought perturbation, and show that these effects may not be mitigated by the trophic complexity of soil communities, at least at the level manipulated in this experiment.

Changes in root-exudate-induced respiration reveal a novel mechanism through which drought affects ecosystem carbon cycling.

Root exudates play an important role in ecosystem response to climate change, but the functional consequences of drought-induced changes in the quality of root exudates are unknown. Here, we addressed this knowledge gap in a unique experimental approach. We subjected two common grassland species that differ widely in their growth strategies and root systems, the grass Holcus lanatus and the forb Rumex acetosa, to 2 wk of drought. We collected root exudates and soils at the end of the drought and after 2 wk of recovery and readded all root exudates to all soils in a fully reciprocal set-up to measure root-exudate-induced respiration. We found that soil treatment was unimportant for determining root-exudate-induced respiration. By contrast, root exudates collected from plants that had experienced drought clearly triggered more soil respiration than exudates from undroughted plants. Importantly, this increased respiration compensated for the lower rates of root exudation in droughted plants. Our findings reveal a novel mechanism through which drought can continue to affect ecosystem carbon cycling, and a potential plant strategy to facilitate regrowth through stimulating microbial activity. These findings have important implications for understanding plant and ecosystem response to drought.