Microbiome-mediated alleviation of tobacco replant problem via autotoxin degradation after long-term continuous cropping.

Continuous cropping often results in severe "replant problem," across various crops due to the autotoxins accumulation, soil acidification, pathogens proliferation, and microbial dysfunction. We unveiled a groundbreaking phenomenon that long-term continuous cropping (LTCC) can alleviate the tobacco replant problem. This mitigation occurs through the enrichment of autotoxin-degrading microbes, and the transformative impact is evident with even a modest application (10%) of LTCC soil to short-term continuous cropping (STCC) soil. Our investigation has pinpointed specific autotoxin-degrading bacteria, particularly the Pseudomonas and Burkholderia species, which exhibit the capacity to alleviate the tobacco replant problem in STCC soil. Their autotoxin-degrading mechanism using axenic culture and soil samples was also conducted via comprehensive analyses of microbiome and transcriptome approach. This research sheds light on the potential of LTCC as a strategic approach for sustainable agriculture, addressing replant problems and promoting the health of cropping systems. UV, ultraviolet; OD, optical density.

Belowground cascading biotic interactions trigger crop diversity benefits.

Crop diversification practices offer numerous synergistic benefits. So far, research has traditionally been confined to exploring isolated, unidirectional single-process interactions among plants, soil, and microorganisms. Here, we present a novel and systematic perspective, unveiling the intricate web of plant-soil-microbiome interactions that trigger cascading effects. Applying the principles of cascading interactions can be an alternative way to overcome soil obstacles such as soil compaction and soil pathogen pressure. Finally, we introduce a research framework comprising the design of diversified cropping systems by including commercial varieties and crops with resource-efficient traits, the exploration of cascading effects, and the innovation of field management. We propose that this provides theoretical and methodological insights that can reveal new mechanisms by which crop diversity increases productivity.

Mimicking natural deterrent strategies in plants using adhesive spheres.

With a continuous increase in world population and food production, chemical pesticide use is growing accordingly, yet unsustainably. As chemical pesticides are harmful to the environment and developmental resistance in pests is increasing, a sustainable and effective pesticide alternative is needed. Inspired by nature, we mimic one defense strategy of plants, glandular trichomes, to shift away from using chemical pesticides by moving toward a physical immobilization strategy via adhesive particles. Through controlled oxidation of a biobased starting material, triglyceride oils, an adhesive material is created while monitoring the reactive intermediates. After being milled into particles, nanoindentation shows these particles to be adhesive even at low contact forces. A suspension of particles is then sprayed and found to be effective at immobilizing a target pest, thrips, Frankliniella occidentalis. Small arthropod pests, like thrips, can cause crop damage through virus transfer, which is prevented by their immobilization. We show that through a scalable fabrication process, biosourced materials can be used to create an effective, sustainable physical pesticide.

Fungal communities are passengers in community development of dune ecosystems, while bacteria are not.

An increasing number of studies of above-belowground interactions provide a fundamental basis for our understanding of the coexistence between plant and soil communities. However, we lack empirical evidence to understand the directionality of drivers of plant and soil communities under natural conditions: 'Are soil microorganisms driving plant community functioning or do they adapt to the plant community?' In a field experiment in an early successional dune ecosystem, we manipulated soil communities by adding living (i.e., natural microbial communities) and sterile soil inocula, originating from natural ecosystems, and examined the annual responses of soil and plant communities. The experimental manipulations had a persistent effect on the soil microbial community with divergent impacts for living and sterile soil inocula. The plant community was also affected by soil inoculation, but there was no difference between the impacts of living and sterile inocula. We also observed an increasing convergence of plant and soil microbial composition over time. Our results show that alterations in soil abiotic and biotic conditions have long-term effects on the composition of both plant and soil microbial communities. Importantly, our study provides direct evidence that soil microorganisms are not "drivers" of plant community dynamics. We found that soil fungi and bacteria manifest different community assemblies in response to treatments. Soil fungi act as "passengers," that is, soil microorganisms reflect plant community dynamics but do not alter it, whereas soil bacteria are neither "drivers" nor "passengers" of plant community dynamics in early successional ecosystems. These results are critical for understanding the community assembly of plant and soil microbial communities under natural conditions and are directly relevant for ecosystem management and restoration.

Impact of intraspecific variation in insect microbiomes on host phenotype and evolution.

Microbes can be an important source of phenotypic plasticity in insects. Insect physiology, behaviour, and ecology are influenced by individual variation in the microbial communities held within the insect gut, reproductive organs, bacteriome, and other tissues. It is becoming increasingly clear how important the insect microbiome is for insect fitness, expansion into novel ecological niches, and novel environments. These investigations have garnered heightened interest recently, yet a comprehensive understanding of how intraspecific variation in the assembly and function of these insect-associated microbial communities can shape the plasticity of insects is still lacking. Most research focuses on the core microbiome associated with a species of interest and ignores intraspecific variation. We argue that microbiome variation among insects can be an important driver of evolution, and we provide examples showing how such variation can influence fitness and health of insects, insect invasions, their persistence in new environments, and their responses to global environmental changes. A and B are two stages of an individual or a population of the same species. The drivers lead to a shift in the insect associated microbial community, which has consequences for the host. The complex interplay of those consequences affects insect adaptation and evolution and influences insect population resilience or invasion.

Effect of organic amendments obtained from different pretreatment technologies on soil microbial community.

The application of organic amendments (OAs) obtained from biological treatment technologies is a common agricultural practice to increase soil functionality and fertility. OAs and their respective pretreatment processes have been extensively studied. However, comparing the properties of OAs obtained from different pretreatment processes remains challenging. In most cases, the organic residues used to produce OAs exhibit intrinsic variability and differ in origin and composition. In addition, few studies have focused on comparing OAs from different pretreatment processes in the soil microbiome, and the extent to which OAs affect the soil microbial community remains unclear. This limits the design and implementation of effective pretreatments aimed at reusing organic residues and facilitating sustainable agricultural practices. In this study, we used the same model residues to produce OAs to enable meaningful comparisons among compost, digestate, and ferment. These three OAs contained different microbial communities. Compost had higher bacterial but lower fungal alpha diversity than ferment and digestate. Compost-associated microbes were more prevalent in the soil than ferment- and digestate-associated microbes. More than 80% of the bacterial ASVs and fungal OTUs from the compost were detected 3 months after incorporation into the soil. However, the addition of compost had less influence on the resulting soil microbial biomass and community composition than the addition of ferment or digestate. Specific native soil microbes, members from Chloroflexi, Acidobacteria, and Mortierellomycota, were absent after ferment and digestate application. The addition of OAs increased the soil pH, particularly in the compost-amended soil, whereas the addition of digestate enhanced the concentrations of dissolved organic carbon (DOC) and available nutrients (such as ammonium and potassium). These physicochemical variables were key factors that influenced soil microbial communities. This study furthers our understanding of the effective recycling of organic resources for the development of sustainable soils.

Growth substrates alter aboveground plant microbial and metabolic properties thereby influencing insect herbivore performance.

The gut microbiome of plant-eaters is affected by the food they eat, but it is currently unclear how the plant metabolome and microbiome are influenced by the substrate the plant grows in and how this subsequently impacts the feeding behavior and gut microbiomes of insect herbivores. Here, we use Plutella xylostella caterpillars and show that the larvae prefer leaves of cabbage plants growing in a vermiculite substrate to those from plants growing in conventional soil systems. From a plant metabolomics analysis, we identified 20 plant metabolites that were related to caterpillar feeding performance. In a bioassay, the effects of these plant metabolites on insects' feeding were tested. Nitrate and compounds enriched with leaves of soilless cultivation promoted the feeding of insects, while compounds enriched with leaves of plants growing in natural soil decreased feeding. Several microbial groups (e.g., Sporolactobacillus, Haliangium) detected inside the plant correlated with caterpillar feeding performance and other microbial groups, such as Ramlibacter and Methylophilus, correlated with the gut microbiome. Our results highlight the role of growth substrates on the food metabolome and microbiome and on the feeding performance and the gut microbiome of plant feeders. It illustrates how belowground factors can influence the aboveground properties of plant-animal systems, which has important implications for plant growth and pest control.

Legacies at work: plant-soil-microbiome interactions underpinning agricultural sustainability.

Agricultural intensification has had long-lasting negative legacies largely because of excessive inputs of agrochemicals (e.g., fertilizers) and simplification of cropping systems (e.g., continuous monocropping). Conventional agricultural management focuses on suppressing these negative legacies. However, there is now increasing attention for creating positive above- and belowground legacies through selecting crop species/genotypes, optimizing temporal and spatial crop combinations, improving nutrient inputs, developing intelligent fertilizers, and applying soil or microbiome inoculations. This can lead to enhanced yields and reduced pest and disease pressure in cropping systems, and can also mitigate greenhouse gas emissions and enhance carbon sequestration in soils. Strengthening positive legacies requires a deeper understanding of plant-soil-microbiome interactions and innovative crop, input, and soil management which can help to achieve agricultural sustainability.

Soil inoculum identity and rate jointly steer microbiomes and plant communities in the field.

Inoculation with soil from different ecosystems can induce changes in plant and soil communities and promote the restoration of degraded ecosystems. However, it is unknown how such inoculations influence the plant and soil communities, how much inoculum is needed, and whether inocula collected from similar ecosystems will steer soil and plant communities in different directions. We conducted a three-year soil inoculation experiment at a degraded grassland and used two different soil inocula both from grasslands with three inoculation rates. We measured the development of the soil and plant communities over a period of three years. Our results show that soil inoculation steers the soil microbiome and plant communities at the inoculated site into different directions and these effects were stronger with higher amount of soil used to inoculate. Network analyses showed that inoculation with upland meadow soil introduced more genera occupying the central position in the biotic network and resulted in more complex networks in the soil than inoculation with meadow steppe soil. Our findings emphasize that there are specific effects of donor soil on soil microbiomes as well as plant communities and that the direction and speed of development depend on the origin and the amount of soil inoculum used. Our findings have important implications for the restoration of biodiversity and ecosystem functioning in degraded grassland ecosystems.

Persistence of plant-mediated microbial soil legacy effects in soil and inside roots.

Plant-soil feedbacks are shaped by microbial legacies that plants leave in the soil. We tested the persistence of these legacies after subsequent colonization by the same or other plant species using 6 typical grassland plant species. Soil fungal legacies were detectable for months, but the current plant effect on fungi amplified in time. By contrast, in bacterial communities, legacies faded away rapidly and bacteria communities were influenced strongly by the current plant. However, both fungal and bacterial legacies were conserved inside the roots of the current plant species and their composition significantly correlated with plant growth. Hence, microbial soil legacies present at the time of plant establishment play a vital role in shaping plant growth even when these legacies have faded away in the soil due the growth of the current plant species. We conclude that soil microbiome legacies are reversible and versatile, but that they can create plant-soil feedbacks via altering the endophytic community acquired during early ontogeny.

Novel chemicals engender myriad invasion mechanisms.

Non-native invasive species (NIS) release chemicals into the environment that are unique to the invaded communities, defined as novel chemicals. Novel chemicals impact competitors, soil microbial communities, mutualists, plant enemies, and soil nutrients differently than in the species' native range. Ecological functions of novel chemicals and differences in functions between the native and non-native ranges of NIS are of immense interest to ecologists. Novel chemicals can mediate different ecological, physiological, and evolutionary mechanisms underlying invasion hypotheses. Interactions amongst the NIS and resident species including competitors, soil microbes, and plant enemies, as well as abiotic factors in the invaded community are linked to novel chemicals. However, we poorly understand how these interactions might enhance NIS performance. New empirical data and analyses of how novel chemicals act in the invaded community will fill major gaps in our understanding of the chemistry of biological invasions. A novel chemical-invasion mechanism framework shows how novel chemicals engender invasion mechanisms beyond plant-plant or plant-microorganism interactions.

Plant-Soil Feedbacks and Temporal Dynamics of Plant Diversity-Productivity Relationships.

Plant-soil feedback (PSF) and diversity-productivity relationships are important research fields to study drivers and consequences of changes in plant biodiversity. While studies suggest that positive plant diversity-productivity relationships can be explained by variation in PSF in diverse plant communities, key questions on their temporal relationships remain. Here, we discuss three processes that change PSF over time in diverse plant communities, and their effects on temporal dynamics of diversity-productivity relationships: spatial redistribution and changes in dominance of plant species; phenotypic shifts in plant traits; and dilution of soil pathogens and increase in soil mutualists. Disentangling these processes in plant diversity experiments will yield new insights into how plant diversity-productivity relationships change over time.

Quantitative comparison between the rhizosphere effect of Arabidopsis thaliana and co-occurring plant species with a longer life history.

As a model for genetic studies, Arabidopsis thaliana (Arabidopsis) offers great potential to unravel plant genome-related mechanisms that shape the root microbiome. However, the fugitive life history of this species might have evolved at the expense of investing in capacity to steer an extensive rhizosphere effect. To determine whether the rhizosphere effect of Arabidopsis is different from other plant species that have a less fugitive life history, we compared the root microbiome of Arabidopsis to eight other, later succession plant species from the same habitat. The study included molecular analysis of soil, rhizosphere, and endorhizosphere microbiome both from the field and from a laboratory experiment. Molecular analysis revealed that the rhizosphere effect (as quantified by the number of enriched and depleted bacterial taxa) was ~35% lower than the average of the other eight species. Nevertheless, there are numerous microbial taxa differentially abundant between soil and rhizosphere, and they represent for a large part the rhizosphere effects of the other plants. In the case of fungal taxa, the number of differentially abundant taxa in the Arabidopsis rhizosphere is 10% of the other species' average. In the plant endorhizosphere, which is generally more selective, the rhizosphere effect of Arabidopsis is comparable to other species, both for bacterial and fungal taxa. Taken together, our data imply that the rhizosphere effect of the Arabidopsis is smaller in the rhizosphere, but equal in the endorhizosphere when compared to plant species with a less fugitive life history.

Plant community composition steers grassland vegetation via soil legacy effects.

Soil legacy effects are commonly highlighted as drivers of plant community dynamics and species co-existence. However, experimental evidence for soil legacy effects of conditioning plant communities on responding plant communities under natural conditions is lacking. We conditioned 192 grassland plots using six different plant communities with different ratios of grasses and forbs and for different durations. Soil microbial legacies were evident for soil fungi, but not for soil bacteria, while soil abiotic parameters did not significantly change in response to conditioning. The soil legacies affected the composition of the succeeding vegetation. Plant communities with different ratios of grasses and forbs left soil legacies that negatively affected succeeding plants of the same functional type. We conclude that fungal-mediated soil legacy effects play a significant role in vegetation assembly of natural plant communities.

Soil Inoculation Alters Leaf Metabolic Profiles in Genetically Identical Plants.

Abiotic and biotic properties of soil can influence growth and chemical composition of plants. Although it is well-known that soil microbial composition can vary greatly spatially, how this variation affects plant chemical composition is poorly understood. We grew genetically identical Jacobaea vulgaris in sterilized soil inoculated with live soil collected from four natural grasslands and in 100% sterilized soil. Within each grassland we sampled eight plots, totalling 32 different inocula. Two samples per plot were collected, leading to three levels of spatial variation: within plot, between and within grasslands. The leaf metabolome was analysed with 1H Nuclear magnetic resonance spectroscopy (NMR) to investigate if inoculation altered the metabolome of plants and how this varied between and within grasslands. Inoculation led to changes in metabolomics profiles of J. vulgaris in two out of four sites. Plants grown in sterilized and inoculated soils differed in concentrations of malic acid, tyrosine, trehalose and two pyrrolizidine alkaloids (PA). Metabolomes of plants grown in inoculated soils from different sites varied in glucose, malic acid, trehalose, tyrosine and in one PA. The metabolome of plants grown in soils with inocula from the same site was more similar than with inocula from distant sites. We show that soil influences leaf metabolomes. Performance of aboveground insects often depends on chemical composition of plants. Hence our results imply that soil microbial communities, via affecting aboveground plant metabolomes, can impact aboveground plant-insect food chains but that it is difficult to make general predictions due to spatial variation in soil microbiomes.

Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities.

BACKGROUND: Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly. The origin and functionality of insect microbiomes is not well understood. Many caterpillars can harbor symbionts in their gut that impact host metabolism, nutrient uptake and pathogen protection. Despite our lack of knowledge on the ecological factors driving microbiome assemblages of wild caterpillars, they seem to be highly variable and influenced by diet and environment. Several recent studies have shown that shoot-feeding caterpillars acquire part of their microbiome from the soil. Here, we examine microbiomes of a monophagous caterpillar (Tyria jacobaeae) collected from their natural host plant (Jacobaea vulgaris) growing in three different environments: coastal dunes, natural inland grasslands and riverine grasslands, and compare the bacterial communities of the wild caterpillars to those of soil samples collected from underneath each of the host plants from which the caterpillars were collected. RESULTS: The microbiomes of the caterpillars were dominated by Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. Only 5% of the total bacterial diversity represented 86.2% of the total caterpillar's microbiome. Interestingly, we found a high consistency of dominant bacteria within the family Burkholderiaceae in all caterpillar samples across the three habitats. There was one amplicon sequence variant belonging to the genus Ralstonia that represented on average 53% of total community composition across all caterpillars. On average, one quarter of the caterpillar microbiome was shared with the soil. CONCLUSIONS: We found that the monophagous caterpillars collected from fields located more than 100 km apart were all dominated by a single Ralstonia. The remainder of the bacterial communities that were present resembled the local microbial communities in the soil in which the host plant was growing. Our findings provide an example of a caterpillar that has just a few key associated bacteria, but that also contains a community of low abundant bacteria characteristic of soil communities.

Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest.

Soils and their microbiomes are now recognized as key components of plant health, but how to steer those microbiomes to obtain their beneficial functions is still unknown. Here, we assess whether plant-soil feedbacks can be applied in a crop system to shape soil microbiomes that suppress herbivorous insects in above-ground tissues. We used four grass and four forb species to condition living soil. Then we inoculated those soil microbiomes into sterilized soil and grew chrysanthemum as a focal plant. We evaluated the soil microbiome in the inocula and after chrysanthemum growth, as well as plant and herbivore parameters. We show that inocula and inoculated soil in which a focal plant had grown harbor remarkably different microbiomes, with the focal plant exerting a strong negative effect on fungi, especially arbuscular mycorrhizal fungi. Soil inoculation consistently induced resistance against the thrips Frankliniella occidentalis, but not against the mite Tetranychus urticae, when compared with sterilized soil. Additionally, plant species shaped distinct microbiomes that had different effects on thrips, chlorogenic acid concentrations in leaves and plant growth. This study provides a proof-of-concept that the plant-soil feedback concept can be applied to steer soil microbiomes with the goal of inducing resistance above ground against herbivorous insects.

Structure and ecological function of the soil microbiome affecting plant-soil feedbacks in the presence of a soil-borne pathogen.

Interactions between plants and soil microbes are important for plant growth and resistance. Through plant-soil-feedbacks, growth of a plant is influenced by the previous plant that was growing in the same soil. We performed a plant-soil feedback study with 37 grass, forb and legume species, to condition the soil and then tested the effects of plant-induced changes in soil microbiomes on the growth of the commercially important cut-flower Chrysanthemum in presence and absence of a pathogen. We analysed the fungal and bacterial communities in these soils using next-generation sequencing and examined their relationship with plant growth in inoculated soils with or without the root pathogen, Pythium ultimum. We show that a large part of the soil microbiome is plant species-specific while a smaller part is conserved at the plant family level. We further identified clusters of plant species creating plant growth promoting microbiomes that suppress concomitantly plant pathogens. Especially soil inocula with higher relative abundances of arbuscular mycorrhizal fungi caused positive effects on the Chrysanthemum growth when exposed to the pathogen. We conclude that plants differ greatly in how they influence the soil microbiome and that plant growth and protection against pathogens is associated with a complex soil microbial community.

Time after Time: Temporal Variation in the Effects of Grass and Forb Species on Soil Bacterial and Fungal Communities.

Microorganisms are found everywhere and have critical roles in most ecosystems, but compared to plants and animals, little is known about their temporal dynamics. Here, we investigated the temporal stability of bacterial and fungal communities in the soil and how their temporal variation varies between grasses and forb species. We established 30 outdoor mesocosms consisting of six plant monocultures and followed microbial communities for an entire year in these soils. We demonstrate that bacterial communities vary greatly over time and that turnover plays an important role in shaping microbial communities. We further show that bacterial communities rapidly shift from one state to another and that this is related to changes in the relative contribution of certain taxa rather than to extinction. Fungal soil communities are more stable over time, and a large part of the variation can be explained by plant species and by whether they are grasses or forbs. Our findings show that the soil bacterial community is shaped by time, while plant group and plant species-specific effects drive soil fungal communities. This has important implications for plant-soil research and highlights that temporal dynamics of soil communities cannot be ignored in studies on plant-soil feedback and microbial community composition and function.IMPORTANCE Our findings highlight how soil fungal and bacterial communities respond to time, season, and plant species identity. We found that succession shapes the soil bacterial community, while plant species and the type of plant species that grows in the soil drive the assembly of soil fungal communities. Future research on the effects of plants on soil microbes should take into consideration the relative roles of both time and plant growth on creating soil legacies that impact future plants growing in the soil. Understanding the temporal (in)stability of microbial communities in soils will be crucial for predicting soil microbial composition and functioning, especially as plant species compositions will shift with global climatic changes and land-use alterations. As fungal and bacterial communities respond to different environmental cues, our study also highlights that the selection of study organisms to answer specific ecological questions is not trivial and that the timing of sampling can greatly affect the conclusions made from these studies.