jenatron-an-experimental-approach-to-study-effects-plant-history-soil

JenaTron - An Experimental Approach to Study the Effects of Plant History and Soil History on Grassland Ecosystem Functioning

The global loss of biodiversity has motivated many studies that experimentally vary plant species richness and examine the consequences for ecosystem ...

University of Amsterdam

Stool microRNA profiling- dumpster diving for a master marker?

Water deficit tolerance is critical for plant fitness and survival, especially when successive drought events happen. Specific soil microorganisms are however able to improve plant tolerance to stresses, such as those displaying a 1-aminocyclopropane-1-carboxylate (ACC) deaminase activity. Microorganisms adapted to dry conditions can be selected by plants over time because of properties such as sporulation, substrate preference, or cell-wall thickness. However, the complexity and interconnection between abiotic factors, like drought or soil management, and biotic factors, like plant species identity, make it difficult to elucidate the general selection processes of such microorganisms. Using a pot experiment in which wheat and barley were grown on conventional and organic farming soils, we determined the effect of water deficit history on soil microorganisms by comparing single and successive events of water limitation. The analysis showed that water deficit strongly impacts the composition of both the total microbial community (16S rRNA genes) and one of ACC deaminase-positive ( ) microorganisms in the rhizosphere. In contrast, successive dry conditions moderately influence the abundance and diversity of both communities compared to a single dry event. We revealed interactive effects of the farming soil type and the water deficit conditioning treatment. Indeed, possibly due to better nutrient status, plants grown on soils from conventional farming showed higher growth and were able to select more adapted microbial taxa. Some of them are already known for their plant-beneficial properties like the Actinobacteria , but interestingly, some Proteobacteria were also enriched after a water deficit history under conventional farming. Our approach allowed us to identify key microbial taxa promoting drought adaptation of cereals, thus improving our understanding of drought effects on plant-microbe interactions.

Water Deficit History Selects Plant Beneficial Soil Bacteria Differently Under Conventional and Organic Farming.

Depending on their tree species composition, forests recruit different soil microbial communities. Likewise, the vertical nutrient gradient along soil profiles impacts these communities and their activities. In forest soils, bacteria and fungi commonly compete, coexist, and interact, which is challenging for understanding the complex mechanisms behind microbial structuring. Using amplicon sequencing, we analyzed bacterial and fungal diversity in relation to forest composition and soil depth. Moreover, employing random forest models, we identified microbial indicator taxa of forest plots composed of either deciduous or evergreen trees, or their mixtures, as well as of three soil depths. We expected that forest composition and soil depth affect bacterial and fungal diversity and community structure differently. Indeed, relative abundances of microbial communities changed more across soil depths than in relation to forest composition. The microbial Shannon diversity was particularly affected by soil depth and by the proportion of evergreen trees. Our results also reflected that bacterial communities are primarily shaped by soil depth, while fungi were influenced by forest tree species composition. An increasing proportion of evergreen trees did not provoke differences in main bacterial metabolic functions, e.g., carbon fixation, degradation, or photosynthesis. However, significant responses related to specialized bacterial metabolisms were detected. Saprotrophic, arbuscular mycorrhizal, and plant pathogenic fungi were related to the proportion of evergreen trees, particularly in topsoil. Prominent microbial indicator taxa in the deciduous forests were characterized to be r-strategists, whereas K-strategists dominated evergreen plots. Considering simultaneously forest composition and soil depth to unravel differences in microbial communities, metabolic pathways and functional guilds have the potential to enlighten mechanisms that maintain forest soil functionality and provide resistance against disturbances.

Effects of Tree Composition and Soil Depth on Structure and Functionality of Belowground Microbial Communities in Temperate European Forests.

The reconstruction of genomes is a critical step in genome-resolved metagenomics and for multi-omic data integration from microbial communities. Here, we present binny, a binning tool that produces high-quality metagenome-assembled genomes (MAG) from both contiguous and highly fragmented genomes. Based on established metrics, binny outperforms or is highly competitive with commonly used and state-of-the-art binning methods and finds unique genomes that could not be detected by other methods. binny uses k-mer-composition and coverage by metagenomic reads for iterative, nonlinear dimension reduction of genomic signatures as well as subsequent automated contig clustering with cluster assessment using lineage-specific marker gene sets. When compared with seven widely used binning algorithms, binny provides substantial amounts of uniquely identified MAGs and almost always recovers the most near-complete ($\gt 95\%$ pure, $\gt 90\%$ complete) and high-quality ($\gt 90\%$ pure, $\gt 70\%$ complete) genomes from simulated datasets from the Critical Assessment of Metagenome Interpretation initiative, as well as substantially more high-quality draft genomes, as defined by the Minimum Information about a Metagenome-Assembled Genome standard, from a real-world benchmark comprised of metagenomes from various environments than any other tested method.

binny: an automated binning algorithm to recover high-quality genomes from complex metagenomic datasets.

Understanding the biological roles of root hairs is key to projecting their contributions to plant growth and to assess their relevance for plant breeding. The objective of this study was to assess the importance of root hairs for maize nutrition, carbon allocation and root gene expression in a field experiment. Applying wild type and root hairless  maize grown on loam and sand, we examined the period of growth including 4-leaf, 9-leaf and tassel emergence stages, accompanied with a low precipitation rate.  maize had lower shoot growth and lower total amounts of mineral nutrients than wild type, but the concentrations of mineral elements, root gene expression, or carbon allocation were largely unchanged. For these parameters, growth stage accounted for the main differences, followed by substrate. Substrate-related changes were pronounced during tassel emergence, where the concentrations of several elements in leaves as well as cell wall formation-related root gene expression and C allocation decreased. In conclusion, the presence of root hairs stimulated maize shoot growth and total nutrient uptake, but other parameters were more impacted by growth stage and soil texture. Further research should relate root hair functioning to the observed losses in maize productivity and growth efficiency.

Plant Age and Soil Texture Rather Than the Presence of Root Hairs Cause Differences in Maize Resource Allocation and Root Gene Expression in the Field.

The measurement of uncharacterized pools of biological molecules through techniques such as metabarcoding, metagenomics, metatranscriptomics, metabolomics, and metaproteomics produces large, multivariate datasets. Analyses of these datasets have successfully been borrowed from community ecology to characterize the molecular diversity of samples (ɑ-diversity) and to assess how these profiles change in response to experimental treatments or across gradients (β-diversity). However, sample preparation and data collection methods generate biases and noise which confound molecular diversity estimates and require special attention. Here, we examine how technical biases and noise that are introduced into multivariate molecular data affect the estimation of the components of diversity (i.e., total number of different molecular species, or entities; total number of molecules; and the abundance distribution of molecular entities). We then explore under which conditions these biases affect the measurement of ɑ- and β-diversity and highlight how novel methods commonly used in community ecology can be adopted to improve the interpretation and integration of multivariate molecular data. Video Abstract.

The community ecology perspective of omics data.

Root-associated fungi could play a role in determining both the positive relationship between plant diversity and productivity in experimental grasslands, and its strengthening over time. This hypothesis assumes that specialized pathogenic and mutualistic fungal communities gradually assemble over time, enhancing plant growth more in species-rich than in species-poor plots. To test this hypothesis, we used high-throughput amplicon sequencing to characterize root-associated fungal communities in experimental grasslands of 1 and 15 years of age with varying levels of plant species richness. Specifically, we tested whether the relationship between fungal communities and plant richness and productivity becomes stronger with the age of the experimental plots. Our results showed that fungal diversity increased with plant diversity, but this relationship weakened rather than strengthened over the two time points. Contrastingly, fungal community composition showed increasing associations with plant diversity over time, suggesting a gradual build-up of specific fungal assemblages. Analyses of different fungal guilds showed that these changes were particularly marked in pathogenic fungi, whose shifts in relative abundance are consistent with the pathogen dilution hypothesis in diverse plant communities. Our results suggest that root-associated fungal pathogens play more specific roles in determining the diversity-productivity relationship than other root-associated plant symbionts.

The structure of root-associated fungal communities is related to the long-term effects of plant diversity on productivity.

Potential of microbiome-based solutions for agrifood systems.

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.

Root cap is an important determinant of rhizosphere microbiome assembly.

The increasing frequency of extreme weather events highlights the need to understand how soil microbiomes respond to such disturbances. Here, metagenomics was used to investigate the effects of future climate scenarios (+0.6 °C warming and altered precipitation) on soil microbiomes during the summers of 2014-2019. Unexpectedly, Central Europe experienced extreme heatwaves and droughts during 2018-2019, causing significant impacts on the structure, assembly, and function of soil microbiomes. Specifically, the relative abundance of Actinobacteria (bacteria), Eurotiales (fungi), and Vilmaviridae (viruses) was significantly increased in both cropland and grassland. The contribution of homogeneous selection to bacterial community assembly increased significantly from 40.0% in normal summers to 51.9% in extreme summers. Moreover, genes associated with microbial antioxidant (Ni-SOD), cell wall biosynthesis (glmSMU, murABCDEF), heat shock proteins (GroES/GroEL, Hsp40), and sporulation (spoIID, spoVK) were identified as potential contributors to drought-enriched taxa, and their expressions were confirmed by metatranscriptomics in 2022. The impact of extreme summers was further evident in the taxonomic profiles of 721 recovered metagenome-assembled genomes (MAGs). Annotation of contigs and MAGs suggested that Actinobacteria may have a competitive advantage in extreme summers due to the biosynthesis of geosmin and 2-methylisoborneol. Future climate scenarios caused a similar pattern of changes in microbial communities as extreme summers, but to a much lesser extent. Soil microbiomes in grassland showed greater resilience to climate change than those in cropland. Overall, this study provides a comprehensive framework for understanding the response of soil microbiomes to extreme summers.

Extreme summers impact cropland and grassland soil microbiomes.

Recent studies on root traits have shown that there are two axes explaining trait variation belowground: the collaboration axis with mycorrhizal partners and the conservation ('fast - slow') axis. However, it is yet unknown whether these trait axes affect the assembly of soilborne fungi. We expect saprotrophic fungi to link to the conservation axis of root traits, whereas pathogenic and arbuscular mycorrhizal fungi link to the collaboration axis, but in opposite directions, as arbuscular mycorrhizal fungi might provide pathogen protection. To test these hypotheses, we sequenced rhizosphere fungal communities and measured root traits in monocultures of 25 grassland plant species, differing in age. Within the fungal guilds, we evaluated fungal species richness, relative abundance and community composition. Contrary to our hypotheses, fungal diversity and relative abundance were not strongly related to the root trait axes. However, saprotrophic fungal community composition was affected by the conservation gradient and pathogenic community composition by the collaboration gradient. The rhizosphere AMF community composition did not change along the collaboration gradient, even though the root trait axis was in line with the root mycorrhizal colonization rate. Overall, our results indicate that in the long term, the root trait axes are linked with fungal community composition.

Responses of rhizosphere fungi to the root economics space in grassland monocultures of different age.

Gut microbiome differences between people with Parkinson's disease (PD) and control subjects without Parkinsonism are widely reported, but potential alterations related to PD with mild cognitive impairment (MCI) have yet to be comprehensively explored. We compared gut microbial features of PD with MCI (n = 58) to cognitively unimpaired PD (n = 60) and control subjects (n = 90) with normal cognition. Our results did not support a specific microbiome signature related to MCI in PD.

Gut microbiome is not associated with mild cognitive impairment in Parkinson's disease.

Soil ammonia-oxidizing archaea (AOA) play a crucial role in converting ammonia to nitrite, thereby mobilizing reactive nitrogen species into their soluble form, with a significant impact on nitrogen losses from terrestrial soils. Yet, our knowledge regarding their diversity and functions remains limited. In this study, we reconstructed 97 high-quality AOA metagenome-assembled genomes (MAGs) from 180 soil samples collected in Central Germany during 2014-2019 summers. These MAGs were affiliated with the order Nitrososphaerales and clustered into four family-level clades (NS-α/γ/δ/ε). Among these MAGs, 75 belonged to the most abundant but least understood δ-clade. Within the δ-clade, the amoA genes in three MAGs from neutral soils showed a 99.5% similarity to the fosmid clone 54d9, which has served as representative of the δ-clade for the past two decades since even today no cultivated representatives are available. Seventy-two MAGs constituted a distinct δ sub-clade, and their abundance and expression activity were more than twice that of other MAGs in slightly acidic soils. Unlike the less abundant clades (α, γ, and ε), the δ-MAGs possessed multiple highly expressed intracellular and extracellular carbohydrate-active enzymes responsible for carbohydrate binding (CBM32) and degradation (GH5), along with highly expressed genes involved in ammonia oxidation. Together, these results suggest metabolic versatility of uncultured soil AOA and a potential mixotrophic or chemolithoheterotrophic lifestyle among 54d9-like AOA.

Metabolic potential of Nitrososphaera-associated clades.

Despite mounting evidence of their importance in human health and ecosystem functioning, the definition and measurement of 'healthy microbiomes' remain unclear. More advanced knowledge exists on health associations for compounds used or produced by microbes. Environmental microbiome exposures (especially via soils) also help shape, and may supplement, the functional capacity of human microbiomes. Given the synchronous interaction between microbes, their feedstocks, and micro-environments, with functional genes facilitating chemical transformations, our objective was to examine microbiomes in terms of their capacity to process compounds relevant to human health. Here we integrate functional genomics and biochemistry frameworks to derive new quantitative measures of in silico potential for human gut and environmental soil metagenomes to process a panel of major compound classes (e.g., lipids, carbohydrates) and selected biomolecules (e.g., vitamins, short-chain fatty acids) linked to human health. Metagenome functional potential profile data were translated into a universal compound mapping 'landscape' based on bioenergetic van Krevelen mapping of function-level meta-compounds and corresponding functional relative abundances, reflecting imprinted genetic capacity of microbiomes to metabolize an array of different compounds. We show that measures of 'compound processing potential' associated with human health and disease (examining atherosclerotic cardiovascular disease, colorectal cancer, type 2 diabetes and anxious-depressive behavior case studies), and displayed seemingly predictable shifts along gradients of ecological disturbance in plant-soil ecosystems (three case studies). Ecosystem quality explained 60-92 % of variation in soil metagenome compound processing potential measures in a post-mining restoration case study dataset. With growing knowledge of the varying proficiency of environmental microbiota to process human health associated compounds, we might design environmental interventions or nature prescriptions to modulate our exposures, thereby advancing microbiota-oriented approaches to human health. Compound processing potential offers a simplified, integrative approach for applying metagenomics in ongoing efforts to understand and quantify the role of microbiota in environmental- and human-health.

Bioenergetic mapping of 'healthy microbiomes' via compound processing potential imprinted in gut and soil metagenomes.

Ecosystem functioning depends on biodiversity at multiple trophic levels, yet relationships between multitrophic diversity and ecosystem multifunctionality have been poorly explored, with studies often focusing on individual trophic levels and functions and on specific ecosystem types. Here, we show that plant diversity can affect ecosystem functioning both directly and by affecting other trophic levels. Using data on 13 trophic groups and 13 ecosystem functions from two large biodiversity experiments-one representing temperate grasslands and the other subtropical forests-we found that plant diversity increases multifunctionality through elevated multitrophic diversity. Across both experiments, the association between multitrophic diversity and multifunctionality was stronger than the relationship between the diversity of individual trophic groups and multifunctionality. Our results also suggest that the role of multitrophic diversity is greater in forests than in grasslands. These findings imply that, to promote sustained ecosystem multifunctionality, conservation planning must consider the diversity of both plants and higher trophic levels.

Plant diversity enhances ecosystem multifunctionality via multitrophic diversity.

Gingivitis-the inflammation of the gums-is a reversible stage of periodontal disease. It is caused by dental plaque formation due to poor oral hygiene. However, gingivitis susceptibility involves a complex set of interactions between the oral microbiome, oral metabolome and the host. In this study, we investigated the dynamics of the oral microbiome and its interactions with the salivary metabolome during experimental gingivitis in a cohort of 41 systemically healthy participants. We use Parallel Factor Analysis (PARAFAC), which is a multi-way generalization of Principal Component Analysis (PCA) that can model the variability in the response due to subjects, variables and time. Using the modelled responses, we identified microbial subcommunities with similar dynamics that connect to the magnitude of the gingivitis response. By performing high level integration of the predicted metabolic functions of the microbiome and salivary metabolome, we identified pathways of interest that describe the changing proportions of Gram-positive and Gram-negative microbiota, variation in anaerobic bacteria, biofilm formation and virulence.

Multi-way modelling of oral microbial dynamics and host-microbiome interactions during induced gingivitis.

Trait-based approaches have been increasingly used to relate plants to soil microbial communities. Using the recently described root economics space as an approach to explain the structure of soil-borne fungal communities, our study in a grassland diversity experiment reveals distinct root trait strategies at the plant community level. In addition to significant effects of plant species richness, we show that the collaboration and conservation gradient are strong drivers of the composition of the different guilds of soil fungi. Saprotrophic fungi are most diverse in species-rich plant communities with 'slow' root traits, whereas plant pathogenic fungi are most diverse and abundant in communities with 'fast' and 'DIY' root traits. Fungal biomass is strongly driven by plant species richness. Our results illustrate that the root economics space and plant species richness jointly determine the effects of plants on soil fungal communities and their potential role in plant fitness and ecosystem functioning.

Article	Year
Stool microRNA profiling- dumpster diving for a master marker? Gut\| PubMed ID: 34479951	2022
Water Deficit History Selects Plant Beneficial Soil Bacteria Differently Under Conventional and Organic Farming. Frontiers in microbiology\| PubMed ID: 35770171	2022
Effects of Tree Composition and Soil Depth on Structure and Functionality of Belowground Microbial Communities in Temperate European Forests. Frontiers in microbiology\| PubMed ID: 35910637	2022
binny: an automated binning algorithm to recover high-quality genomes from complex metagenomic datasets. Briefings in bioinformatics\| PubMed ID: 36239393	2022
Plant Age and Soil Texture Rather Than the Presence of Root Hairs Cause Differences in Maize Resource Allocation and Root Gene Expression in the Field. Plants (Basel, Switzerland)\| PubMed ID: 36365336	2022
The community ecology perspective of omics data. Microbiome\| PubMed ID: 36510248	2022
The structure of root-associated fungal communities is related to the long-term effects of plant diversity on productivity. Molecular ecology\| PubMed ID: 37081579	2023
Potential of microbiome-based solutions for agrifood systems. Nature food\| PubMed ID: 37118595	2022
Root cap is an important determinant of rhizosphere microbiome assembly. The New phytologist\| PubMed ID: 37301991	2023
Extreme summers impact cropland and grassland soil microbiomes. The ISME journal\| PubMed ID: 37419993	2023
Responses of rhizosphere fungi to the root economics space in grassland monocultures of different age. The New phytologist\| PubMed ID: 37691273	2023
Gut microbiome is not associated with mild cognitive impairment in Parkinson's disease. NPJ Parkinson's disease\| PubMed ID: 38582855	2024
Metabolic potential of Nitrososphaera-associated clades. The ISME journal\| PubMed ID: 38742714	2024
Bioenergetic mapping of 'healthy microbiomes' via compound processing potential imprinted in gut and soil metagenomes. The Science of the total environment\| PubMed ID: 38821286	2024
Plant diversity enhances ecosystem multifunctionality via multitrophic diversity. Nature ecology & evolution\| PubMed ID: 39209981	2024
Multi-way modelling of oral microbial dynamics and host-microbiome interactions during induced gingivitis. NPJ biofilms and microbiomes\| PubMed ID: 39300083	2024
Plant Species Richness and the Root Economics Space Drive Soil Fungal Communities. Ecology letters\| PubMed ID: 39737799	2025

Anna Heintz-Buschart

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