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Protists, a crucial part of the soil food web, are increasingly acknowledged as significant influencers of nutrient cycling and plant performance in farmlands. While topographical and climatic factors are often considered to drive microbial communities on a continental scale, higher trophic levels like heterotrophic protists also rely on their food sources. In this context, bacterivores have received more attention than fungivores. Our study explored the connection between the community composition of protists (specifically Rhizaria and Cercozoa) and fungi across 156 cereal fields in Europe, spanning a latitudinal gradient of 3000 km. We employed a machine-learning approach to measure the significance of fungal communities in comparison to bacterial communities, soil abiotic factors, and climate as determinants of the Cercozoa community composition. Our findings indicate that climatic variables and fungal communities are the primary drivers of cercozoan communities, accounting for 70% of their community composition. Structural equation modelling (SEM) unveiled indirect climatic effects on the cercozoan communities through a change in the composition of the fungal communities. Our data also imply that fungivory might be more prevalent among protists than generally believed. This study uncovers a hidden facet of the soil food web, suggesting that the benefits of microbial diversity could be more effectively integrated into sustainable agriculture practices., (© 2024 The Author(s). Environmental Microbiology published by John Wiley & Sons Ltd.)

Plants impact the development of their rhizosphere microbial communities. It is yet unclear to what extent the root cap and specific root zones contribute to microbial community assembly. To test the roles of root caps and root hairs in the establishment of microbiomes along maize roots (Zea mays), we compared the composition of prokaryote (archaea and bacteria) and protist (Cercozoa and Endomyxa) microbiomes of intact or decapped primary roots of maize inbred line B73 with its isogenic root hairless (rth3) mutant. In addition, we tracked gene expression along the root axis to identify molecular control points for an active microbiome assembly by roots. Absence of root caps had stronger effects on microbiome composition than the absence of root hairs and affected microbial community composition also at older root zones and at higher trophic levels (protists). Specific bacterial and cercozoan taxa correlated with root genes involved in immune response. Our results indicate a central role of root caps in microbiome assembly with ripple-on effects affecting higher trophic levels and microbiome composition on older root zones., (© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.)

Land-use intensification is a major driver of biodiversity loss. However, understanding how different components of land use drive biodiversity loss requires the investigation of multiple trophic levels across spatial scales. Using data from 150 agricultural grasslands in central Europe, we assess the influence of multiple components of local- and landscape-level land use on more than 4,000 above- and belowground taxa, spanning 20 trophic groups. Plot-level land-use intensity is strongly and negatively associated with aboveground trophic groups, but positively or not associated with belowground trophic groups. Meanwhile, both above- and belowground trophic groups respond to landscape-level land use, but to different drivers: aboveground diversity of grasslands is promoted by diverse surrounding land-cover, while belowground diversity is positively related to a high permanent forest cover in the surrounding landscape. These results highlight a role of landscape-level land use in shaping belowground communities, and suggest that revised agroecosystem management strategies are needed to conserve whole-ecosystem biodiversity.

Background: Stress-induced hormones are essential for plants to modulate their microbiota and dynamically adjust to the environment. Despite the emphasis of the role of the phytohormone ethylene in the plant physiological response to heterospecific neighbour detection, less is known about how this activated signal mediates focal plant rhizosphere microbiota to enhance plant fitness. Here, using 3 years of peanut (Arachis hypogaea L.), a legume, and cyanide-containing cassava (Manihot esculenta Crantz) intercropping and peanut monocropping field, pot and hydroponic experiments in addition to exogenous ethylene application and soil incubation experiments, we found that ethylene, a cyanide-derived signal, is associated with the chemical identification of neighbouring cassava and the microbial re-assemblage in the peanut rhizosphere., Results: Ethylene production in peanut roots can be triggered by cyanide production of neighbouring cassava plants. This gaseous signal alters the microbial composition and re-assembles the microbial co-occurrence network of peanut by shifting the abundance of an actinobacterial species, Catenulispora sp., which becomes a keystone in the intercropped peanut rhizosphere. The re-assembled rhizosphere microbiota provide more available nutrients to peanut roots and support seed production., Conclusions: Our findings suggest that root ethylene acts as a signal with a dual role. It plays a role in perceiving biochemical cues from interspecific neighbours, and also has a regulatory function in mediating the rhizosphere microbial assembly, thereby enhancing focal plant fitness by improving seed production. This discovery provides a promising direction to develop novel intercropping strategies for targeted manipulations of the rhizosphere microbiome through phytohormone signals. Video abstract.

Despite their importance, how plant communities and soil microorganisms interact to determine the capacity of ecosystems to provide multiple functions simultaneously (multifunctionality) under climate change is poorly known. We conducted a common garden experiment using grassland species to evaluate how plant functional structure and soil microbial (bacteria and protists) diversity and abundance regulate soil multifunctionality responses to joint changes in plant species richness (one, three and six species) and simulated climate change (3°C warming and 35% rainfall reduction). The effects of species richness and climate on soil multifunctionality were indirectly driven via changes in plant functional structure and their relationships with the abundance and diversity of soil bacteria and protists. More specifically, warming selected for the larger and most productive plant species, increasing the average size within communities and leading to reductions in functional plant diversity. These changes increased the total abundance of bacteria that, in turn, increased that of protists, ultimately promoting soil multifunctionality. Our work suggests that cascading effects between plant functional traits and the abundance of multitrophic soil organisms largely regulate the response of soil multifunctionality to simulated climate change, and ultimately provides novel experimental insights into the mechanisms underlying the effects of biodiversity and climate change on ecosystem functioning., (© 2018 John Wiley & Sons Ltd.)

Microplastic is an emerging contaminant of concern in soils globally, probably gradually increasing in soil due to slow degradation. Few studies on microplastic effects on soil biota are available, and no study in a microplastic contamination context has specifically addressed soil protists. Soil protists, a phylogenetically and functionally diverse group of eukaryotic, unicellular soil organisms, are major consumers of bacteria in soils and are potentially important vehicles for the delivery of microplastics into the soil food chain. Here we build a case for focusing research on soil protists by drawing on data from previous, older studies of phagocytosis in protist taxa, which have long made use of polystyrene latex beads (microspheres). Various soil-borne taxa, including ciliates, flagellates and amoebae take up microplastic beads in the size range of a few micrometers. This included filter feeders as well as amoebae which engulf their prey. Discrimination in microplastic particle uptake depended on species, physiological state as well as particle size. Based on the results of the studies we review here, there is now a need to study microplastic effects in a pollution ecology context: this means considering a broad range of particle types under realistic conditions in the soil, and exploring longer-term effects on soil protist communities and functions., (Copyright © 2018 Elsevier Ltd. All rights reserved.)

Interactions occur between two or more organisms affecting each other. Interactions are decisive for the ecology of the organisms. Without direct experimental evidence the analysis of interactions is difficult. Correlation analyses that are based on co-occurrences are often used to approximate interaction. Here, we present a new mathematical model to estimate the interaction strengths between taxa, based on changes in their relative abundances across environmental gradients.

Soil organisms have an important role in aboveground community dynamics and ecosystem functioning in terrestrial ecosystems. However, most studies have considered soil biota as a black box or focussed on specific groups, whereas little is known about entire soil networks. Here we show that during the course of nature restoration on abandoned arable land a compositional shift in soil biota, preceded by tightening of the belowground networks, corresponds with enhanced efficiency of carbon uptake. In mid- and long-term abandoned field soil, carbon uptake by fungi increases without an increase in fungal biomass or shift in bacterial-to-fungal ratio. The implication of our findings is that during nature restoration the efficiency of nutrient cycling and carbon uptake can increase by a shift in fungal composition and/or fungal activity. Therefore, we propose that relationships between soil food web structure and carbon cycling in soils need to be reconsidered.

Background: Seed dressing with pesticides is widely used to protect crop seeds from pest insects and fungal diseases. While there is mounting evidence that especially neonicotinoid seed dressings detrimentally affect insect pollinators, surprisingly little is known on potential side effects on soil biota. We hypothesized that soil organisms would be particularly susceptible to pesticide seed dressings as they get in direct contact with these chemicals. Using microcosms with field soil we investigated, whether seeds treated either with neonicotinoid insecticides or fungicides influence the activity and interaction of earthworms, collembola, protozoa and microorganisms. The full-factorial design consisted of the factor Seed dressing (control vs. insecticide vs. fungicide), Earthworm (no earthworms vs. addition Lumbricus terrestris L.) and collembola (no collembola vs. addition Sinella curviseta Brook). We used commercially available wheat seed material (Triticum aesticum L. cf. Lukullus) at a recommended seeding density of 367 m(-2)., Results: Seed dressings (particularly fungicides) increased collembola surface activity, increased the number of protozoa and reduced plant decomposition rate but did not affect earthworm activity. Seed dressings had no influence on wheat growth. Earthworms interactively affected the influence of seed dressings on collembola activity, whereas collembola increased earthworm surface activity but reduced soil basal respiration. Earthworms also decreased wheat growth, reduced soil basal respiration and microbial biomass but increased soil water content and electrical conductivity., Conclusions: The reported non-target effects of seed dressings and their interactions with soil organisms are remarkable because they were observed after a one-time application of only 18 pesticide treated seeds per experimental pot. Because of the increasing use of seed dressing in agriculture and the fundamental role of soil organisms in agroecosystems these ecological interactions should receive more attention.

16S rRNA genes and transcripts of Acidobacteria were investigated in 57 grassland and forest soils of three different geographic regions. Acidobacteria contributed 9-31% of bacterial 16S rRNA genes whereas the relative abundances of the respective transcripts were 4-16%. The specific cellular 16S rRNA content (determined as molar ratio of rRNA : rRNA genes) ranged between 3 and 80, indicating a low in situ growth rate. Correlations with flagellate numbers, vascular plant diversity and soil respiration suggest that biotic interactions are important determinants of Acidobacteria 16S rRNA transcript abundances in soils. While the phylogenetic composition of Acidobacteria differed significantly between grassland and forest soils, high throughput denaturing gradient gel electrophoresis and terminal restriction fragment length polymorphism fingerprinting detected 16S rRNA transcripts of most phylotypes in situ. Partial least squares regression suggested that chemical soil conditions such as pH, total nitrogen, C : N ratio, ammonia concentrations and total phosphorus affect the composition of this active fraction of Acidobacteria. Transcript abundance for individual Acidobacteria phylotypes was found to correlate with particular physicochemical (pH, temperature, nitrogen or phosphorus) and, most notably, biological parameters (respiration rates, abundances of ciliates or amoebae, vascular plant diversity), providing culture-independent evidence for a distinct niche specialization of different Acidobacteria even from the same subdivision., (© 2013 John Wiley & Sons Ltd and Society for Applied Microbiology.)

Plant residues provide a major source of nitrogen (N) for plant growth. Litter N mineralization varies with litter carbon-to-nitrogen (C-to-N) ratio and presence of bacterial-feeding fauna. We assessed the effect of amoebae, major bacterial feeders in soil, on mineralization of litter of low (high quality) and high C-to-N ratio (low quality) and evaluated consequences for plant growth. We used stable isotopes to determine plant N uptake from litter and plant C partitioning. Stable isotope probing of phospholipid fatty acids was used to follow incorporation of plant C into microorganisms. Amoebae increased plant N uptake independent of litter quality and thereby the biomass of shoots and roots by 33% and 66%, respectively. Plant allocation of total (13)C to roots in low (42%) exceeded that of high-quality litter treatments (26%). Amoebae increased plant allocation of (13)C to roots by 37%. Microbial community structure and incorporation of (13)C into PLFAs varied significantly with litter quality and in the low-quality litter treatment also with the presence of amoebae. Overall, the results suggest that in particular at low nutrient conditions, root-derived C fosters the mobilization of bacterial N by protozoa, thereby increasing plant growth when microorganisms and plants compete for nutrients., (© 2013 Federation of European Microbiological Societies. Published by John Wiley & Sons Ltd. All rights reserved.)

Dead organic matter (OM) is a major source of nitrogen (N) for plants. The majority of plants support N uptake by symbiosis with arbuscular mycorrhizal (AM) fungi. Mineralization of N is regulated by microfauna, in particular, protozoa grazing on bacteria. We hypothesized that AM fungi and protozoa interactively facilitate plant N nutrition from OM. In soil systems consisting of an OM patch and a root compartment, plant N uptake and consequences for plant carbon (C) allocation were investigated using stable isotopes. Protozoa mobilized N by consuming bacteria, and the mobilized N was translocated via AM fungi to the host plant. The presence of protozoa in both the OM and root compartment stimulated photosynthesis and the translocation of C from the host plant via AM fungi into the OM patch. This stimulated microbial activity in the OM patch, plant N uptake from OM and doubled plant growth. The results indicate that protozoa increase plant growth by both mobilization of N from OM and by protozoa-root interactions, resulting in increased C allocation to roots and into the rhizosphere, thereby increasing plant nutrient exploitation. Hence, mycorrhizal plants need to interact with protozoa to fully exploit N resources from OM., (© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.)

In soil, Acidobacteria constitute on average 20% of all bacteria, are highly diverse, and are physiologically active in situ. However, their individual functions and interactions with higher taxa in soil are still unknown. Here, potential effects of land use, soil properties, plant diversity, and soil nanofauna on acidobacterial community composition were studied by cultivation-independent methods in grassland and forest soils from three different regions in Germany. The analysis of 16S rRNA gene clone libraries representing all studied soils revealed that grassland soils were dominated by subgroup Gp6 and forest soils by subgroup Gp1 Acidobacteria. The analysis of a large number of sites (n = 57) by 16S rRNA gene fingerprinting methods (terminal restriction fragment length polymorphism [T-RFLP] and denaturing gradient gel electrophoresis [DGGE]) showed that Acidobacteria diversities differed between grassland and forest soils but also among the three different regions. Edaphic properties, such as pH, organic carbon, total nitrogen, C/N ratio, phosphorus, nitrate, ammonium, soil moisture, soil temperature, and soil respiration, had an impact on community composition as assessed by fingerprinting. However, interrelations with environmental parameters among subgroup terminal restriction fragments (T-RFs) differed significantly, e.g., different Gp1 T-RFs correlated positively or negatively with nitrogen content. Novel significant correlations of Acidobacteria subpopulations (i.e., individual populations within subgroups) with soil nanofauna and vascular plant diversity were revealed only by analysis of clone sequences. Thus, for detecting novel interrelations of environmental parameters with Acidobacteria, individual populations within subgroups have to be considered.

Soil bacteria are heavily consumed by protozoan predators, and many bacteria have evolved defense strategies such as the production of toxic exometabolites. However, the production of toxins is energetically costly and therefore is likely to be adjusted according to the predation risk to balance the costs and benefits of predator defense. We investigated the response of the biocontrol bacterium Pseudomonas fluorescens CHA0 to a common predator, the free-living amoeba Acanthamoeba castellanii. We monitored the effect of the exposure to predator cues or direct contact with the predators on the expression of the phlA, prnA, hcnA, and pltA genes, which are involved in the synthesis of the toxins, 2,4-diacetylphloroglucinol (DAPG), pyrrolnitrin, hydrogen cyanide, and pyoluteorin, respectively. Predator chemical cues led to 2.2-, 2.0-, and 1.2-fold increases in prnA, phlA, and hcnA expression, respectively, and to a 25% increase in bacterial toxicity. The upregulation of the tested genes was related to the antiprotozoan toxicity of the corresponding toxins. Pyrrolnitrin and DAPG had the highest toxicity, suggesting that bacteria secrete a predator-specific toxin cocktail. The response of the bacteria was elicited by supernatants of amoeba cultures, indicating that water-soluble chemical compounds were responsible for induction of the bacterial defense response. In contrast, direct contact of bacteria with living amoebae reduced the expression of the four bacterial toxin genes by up to 50%, suggesting that protozoa can repress bacterial toxicity. The results indicate that predator-prey interactions are a determinant of toxin production by rhizosphere P. fluorescens and may have an impact on its biocontrol potential.

We constructed an experimental model system to study the effects of grazing by a common soil amoeba, Acanthamoeba castellanii, on the composition of bacterial communities in the rhizosphere of Arabidopsis thaliana. Amoebae showed distinct grazing preferences for specific bacterial taxa, which were rapidly replaced by grazing tolerant taxa in a highly reproducible way. The relative proportion of active bacteria increased although bacterial abundance was strongly decreased by amoebae. Specific bacterial taxa had disappeared already two days after inoculation of amoebae. The decrease in numbers was most pronounced in Betaproteobacteria and Firmicutes. In contrast, Actinobacteria, Nitrospira, Verrucomicrobia and Planctomycetes increased. Although other groups, such as betaproteobacterial ammonia oxidizers and Gammaproteobacteria did not change in abundance, denaturing gradient gel electrophoresis with specific primers for pseudomonads (Gammaproteobacteria) revealed both specific changes in community composition as well as shifts in functional genes (gacA) involved in bacterial defence responses. The resulting positive feedback on plant growth in the amoeba treatment confirms that bacterial grazers play a dominant role in structuring bacteria-plant interactions. This is the first detailed study documenting how rapidly protozoan grazers induce shifts in rhizosphere bacterial community composition.

Soil pseudomonads increase their competitiveness by producing toxic secondary metabolites, which inhibit competitors and repel predators. Toxin production is regulated by cell-cell signalling and efficiently protects the bacterial population. However, cell communication is unstable, and natural populations often contain signal blind mutants displaying an altered phenotype defective in exoproduct synthesis. Such mutants are weak competitors, and we hypothesized that their fitness depends on natural communities on the exoproducts of wild-type bacteria, especially defence toxins. We established mixed populations of wild-type and signal blind, non-toxic gacS-deficient mutants of Pseudomonas fluorescens CHA0 in batch and rhizosphere systems. Bacteria were grazed by representatives of the most important bacterial predators in soil, nematodes (Caenorhabditis elegans) and protozoa (Acanthamoeba castellanii). The gacS mutants showed a negative frequency-dependent fitness and could reach up to one-third of the population, suggesting that they rely on the exoproducts of the wild-type bacteria. Both predators preferentially consumed the mutant strain, but populations with a low mutant load were resistant to predation, allowing the mutant to remain competitive at low relative density. The results suggest that signal blind Pseudomonas increase their fitness by exploiting the toxins produced by wild-type bacteria, and that predation promotes the production of bacterial defence compounds by selectively eliminating non-toxic mutants. Therefore, predators not only regulate population dynamics of soil bacteria but also structure the genetic and phenotypic constitution of bacterial communities.

A gradient of microbial diversity in soil was established by inoculating pasteurized soil with microbial populations of different complexity, which were obtained by a combination of soil fumigation and filtering techniques. Four different soil diversity treatments were planted with six different grass species either in monoculture or in polyculture to test how changes of general microbial functions, such as catabolic diversity and nutrient recycling efficiency would affect the performance of the plant communities. Relatively harsh soil treatments were necessary to elicit visible effects on major soil processes such as decomposition and nitrogen cycling due to the high redundancy and resilience of soil microbial communities. The strongest effects of soil diversity manipulations on plant growth occurred in polycultures where interspecific competition between plants was high. In polycultures, soil diversity reduction led to a gradual, linear decline in biomass production of one subordinate grass species (Bromus hordeaceus), which was compensated by increased growth of two intermediate competitors (Aegilops geniculata, B. madritensis). This negative covariance in growth of competing grass species smoothed the effects of soil diversity manipulations at the plant community level. As a result, total shoot biomass production remained constant. Apparently the effects of soil diversity manipulations were buffered because functional redundancy at both, the microbial and the plant community level complemented each other. The results further suggests that small trade-offs in plant fitness due to general functional shifts at the microbial level can be significant for the outcome of competition in plant communities and thus diversity at much larger scales.

Lateral roots are crucial for the plasticity of root responses to environmental conditions in soil. The bacterivorous microfauna has been shown to increase root branching and to foster auxin producing soil bacteria. However, information on modifications of plant internal auxin content by soil bacteria and bacterivores is missing. Therefore, the effects of a rhizosphere bacterial community and a common soil amoeba ( Acanthamoeba castellanii) on root branching and on auxin (indole-3-acetic acid) metabolism in Lepidium sativum and Arabidopsis thaliana were investigated. In a first experimental series, bacteria increased conjugated auxin concentrations in L. sativum shoots, but did not alter free bioactive auxin content nor root branching. In contrast, in presence of soil bacteria plus amoebae free auxin concentrations in shoots and root branching increased, demonstrating that effects of bacteria on auxin metabolism in plants were strongly modified by the bacterivorous amoebae. In a second experiment, A. thaliana reporter plants for auxin (DR5) and cytokinin (ARR5) responded similarly with increased root branching in the presence of amoebae. Surprisingly, in reporter plants cytokinin but not auxin responses were detectable, accompanied by higher soil nitrate concentrations in the presence of amoebae. Likely, increased nitrate concentrations in the rhizosphere led to an accumulation of cytokinin and interactions with free auxin in plants and finally to increased root growth in the presence of amoebae. Altogether, the results show that mutual control mechanisms exist between plant hormone metabolism and microbial signalling, and that effects on hormonal concentrations of plants by free-living bacteria are strongly influenced by bacterial grazers like amoebae. [ABSTRACT FROM AUTHOR]

Soils provide many ecosystem services that are ultimately dependent on the local diversity and belowground abundance of organisms. Soil biodiversity is affected negatively by many threats and there is a perceived policy requirement for the effective biological monitoring of soils at the European level. The aim of this study was to evaluate and recommend policy relevant, cost-effective soil biological indicators for biodiversity and ecosystem function across Europe. A total of 18 potential indicators were selected using a logical-sieve based approach. This paper considers the use of indicators from the ‘top down’ (i.e. concerned with the process of indicator selection), rather than from the ‘bottom up’ detail of how individual indicators perform at specific sites and with specific treatments. The indicators assessed a range of microbial, faunal and functional attributes, newer nucleic acids based techniques, morphological approaches and process based measurements. They were tested at 6 European experimental sites already in operation and chosen according to land-use, climatic zone and differences in land management intensity. These were 4 arable sites, one each in Atlantic, Continental, Mediterranean and Pannonian climate zones, and 2 grassland sites, one each in Atlantic and Continental zones. At each site we sampled three replicated plots of contrasting management intensity and, while the treatments varied from site to site, their disturbance effects were quantified in terms of land use intensity. The field sampling and laboratory analysis were standardised through a combination of ISO protocols, or standard operating procedures if the former were not available. Sites were sampled twice, in autumn 2012 and spring or autumn 2013, with relative costs of the different indicators being determined each time. A breakdown of the cost effectiveness of the indicators showed the expected trade-off between effort required in the field and effort required in the laboratory. All the indicators were able to differentiate between the sites but, as no single indicator was sensitive to all the differences in land use intensity, we suggest that an indicator programme should be based upon a suite of different indicators. For monitoring under the European climatic zones and land uses of this study, indicators for ecosystem functions related to the services of water regulation, C-sequestration and nutrient provision would include a minimum suite of: earthworms; functional genes; and bait lamina. For effective monitoring of biodiversity all taxonomic groups would need to be addressed. [ABSTRACT FROM AUTHOR]