The neglected roles of adjacent natural ecosystems in maintaining bacterial diversity in agroecosystems.

A central aim of community ecology is to understand how local species diversity is shaped. Agricultural activities are reshaping and filtering soil biodiversity and communities; however, ecological processes that structure agricultural communities have often overlooked the role of the regional species pool, mainly owing to the lack of large datasets across several regions. Here, we conducted a soil survey of 941 plots of agricultural and adjacent natural ecosystems (e.g., forest, wetland, grassland, and desert) in 38 regions across diverse climatic and soil gradients to evaluate whether the regional species pool of soil microbes from adjacent natural ecosystems is important in shaping agricultural soil microbial diversity and completeness. Using a framework of multiscales community assembly, we revealed that the regional species pool was an important predictor of agricultural bacterial diversity and explained a unique variation that cannot be predicted by historical legacy, large-scale environmental factors, and local community assembly processes. Moreover, the species pool effects were associated with microbial dormancy potential, where taxa with higher dormancy potential exhibited stronger species pool effects. Bacterial diversity in regions with higher agricultural intensity was more influenced by species pool effects than that in regions with low intensity, indicating that the maintenance of agricultural biodiversity in high-intensity regions strongly depends on species present in the surrounding landscape. Models for community completeness indicated the positive effect of regional species pool, further implying the community unsaturation and increased potential in bacterial diversity of agricultural ecosystems. Overall, our study reveals the indubitable role of regional species pool from adjacent natural ecosystems in predicting bacterial diversity, which has useful implication for biodiversity management and conservation in agricultural systems.

Agricultural tillage practice and rhizosphere selection interactively drive the improvement of soybean plant biomass.

Rhizosphere microbes play key roles in plant growth and productivity in agricultural systems. One of the critical issues is revealing the interaction of agricultural management (M) and rhizosphere selection effects (R) on soil microbial communities, root exudates and plant productivity. Through a field management experiment, we found that bacteria were more sensitive to the M × R interaction effect than fungi, and the positive effect of rhizosphere bacterial diversity on plant biomass existed in the bacterial three two-tillage system. In addition, inoculation experiments demonstrated that the nitrogen cycle-related isolate Stenotrophomonas could promote plant growth and alter the activities of extracellular enzymes N-acetyl- d-glucosaminidase and leucine aminopeptidase in rhizosphere soil. Microbe-metabolites network analysis revealed that hubnodes Burkholderia-Caballeronia-Paraburkholderia and Pseudomonas were recruited by specific root metabolites under the M × R interaction effect, and the inoculation of 10 rhizosphere-matched isolates further proved that these microbes could promote the growth of soybean seedlings. Kyoto Encyclopaedia of Genes and Genomes pathway analysis indicated that the growth-promoting mechanisms of these beneficial genera were closely related to metabolic pathways such as amino acid metabolism, melatonin biosynthesis, aerobactin biosynthesis and so on. This study provides field observation and experimental evidence to reveal the close relationship between beneficial rhizosphere microbes and plant productivity under the M × R interaction effect.

Core phylotypes enhance the resistance of soil microbiome to environmental changes to maintain multifunctionality in agricultural ecosystems.

Agricultural ecosystems are facing increasing environmental changes. Revealing ecological stability of belowground organisms is key to developing management strategies that maintain agricultural ecosystem services in a changing world. Here, we collected soils from adjacent pairs of maize and rice fields along large spatial scale across Eastern and Southeast China to investigate the importance of core microbiota as a predictor of resistance of soil microbiome (e.g. bacteria, fungi and protist) to climate changes and nutrient fertilization, and their effect on multiple ecosystem functions, representing key services for crop growth and health in agro-ecosystems. Soil microbiome in maize soils exhibited stronger resistance than that in rice soils, by considering multiple aspects of the resistance index, for example, community, phylogenetic conservation and network complexity. Community resistance of soil microbiome showed a geographic pattern, with higher resistance at lower latitudes, suggesting their stronger resistance in warmer regions. Particularly, we highlighted the role of core phylotypes in enhancing the community resistance of soil microbiome, which was essential for the maintenance of multifunctionality in agricultural ecosystems. Our results represent a significant advance in linking core phylotypes to community resistance and ecosystem functions, and therefore forecasting agro-ecosystems dynamics in response to ongoing environmental changes. These suggest that core phylotypes should be considered a key factor in enhancing agricultural sustainability and crop productivity under global change scenarios.

Stochastic processes shape the biogeographic variations in core bacterial communities between aerial and belowground compartments of common bean.

Although studies of biogeography in soil bacterial communities have attracted considerable attention, the generality of these patterns along with assembly processes and underlying drivers is poorly understood in the inner tissues of plants. Plant tissues provide unique ecological habitats for microorganisms, which play an essential role in plant performance. Here, we compared core bacterial communities among five soil-plant associated compartments of common bean across five sampling sites in China. Neutral and null modelling consistently suggested that stochastic processes dominated the core community assembly processes and escalated from the belowground compartments to the inner tissues of aerial plant parts. The multiple distance-decay relationships also varied and had flattened patterns in the stem endosphere, which were shaped by distinct environmental factors in each compartment. Coexistence patterns also varied in topological features, in addition with the sparsest networks in the stem endosphere resulted from the interaction with the stochastic processes. This study considerably expanded our understanding of various biogeographic patterns, assembly processes, and the underlying mechanisms of core bacterial communities between aerial and belowground compartments of common bean. That will provide a scientific basis for the reasonable regulation of core bacterial consortia to get better plant performance.

Smaller microorganisms outcompete larger ones in resistance and functional effects under disturbed agricultural ecosystems.

Body size is a key ecological trait of soil microorganisms related to their adaptation to environmental changes. In this study, we reveal that the smaller microorganisms show stronger community resistance than larger organisms in both maize and rice soil. Compared with larger organisms, smaller microorganisms have higher diversity and broader niche breadth to deploy survival strategies, because of which they are less affected by environmental selection and thus survive in complex and various kinds of environments. In addition, the strong correlation between smaller microorganisms and ecosystem functions reflects their greater metabolic flexibility and illustrates their significant roles in adaptation to continuously changing environments. This research highlights the importance of body size in maintaining stability of the soil microbiome and forecasting agroecosystem dynamics under environmental disturbances.

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

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

Oligotrophic microbes are recruited to resist multiple global change factors in agricultural subsoils.

An increasing number of anthropogenic pressures can have negative effects on biodiversity and ecosystem functioning. However, our understanding of how soil microbial communities and functions in response to multiple global change factors (GCFs) is still incomplete, particularly in less frequently disturbed subsoils. In this study, we examined the impact of different levels of GCFs (0-9) on soil functions and bacterial communities in both topsoils (0-20 cm) and subsoils (20-40 cm) of an agricultural ecosystem, and characterized the intrinsic factors influencing community resistance based on microbial life history strategy. Our experimental results showed a decline in soil multifunctionality, bacterial diversity, and community resistance as the number of GCFs increased, with a more drastic reduction in community resistance of subsoils. Specifically, we observed a significantly positive relationship between the oligotroph/copiotroph ratio and community resistance in subsoils, which was also verified by the negative correlation between 16S rRNA operon (rrn) copy number and community resistance. Structural equation modeling further revealed the direct effects of community resistance in promoting the ecosystem functioning, regardless of top- and subsoils. Therefore, these results suggested that subsoils may recruit more oligotrophic microbes to enhance their originally weaker community resistance under multiple GCFs, which was essential for maintaining sustainable agroecological functions and services. Overall, our study represents a significant advance in linking microbial life history strategy to the resistance of belowground microbial community and functionality.

Agricultural Management Drive Bacterial Community Assembly in Different Compartments of Soybean Soil-Plant Continuum.

Flowering stage of soybean is an important agronomic trait, which is important for soybean yield, quality and adaptability, and is the external expression of integrating external environmental factors and endogenous signals of the plant itself. Cropping system can change soil properties and fertility, which in turn determine plant growth and yield. The microbial community is the key regulator of plant health and production performance. Currently, there is limited understanding of the effects of cropping systems on microbial community composition, ecological processes controlling community assembly in different soil-plant continuum compartments of soybean. Here, we hope to clarify the structure and assembly process of different soybean compartments bacterial community at flowering stage through our work. The results showed that intercropping decreased the species diversity of rhizosphere and phyllosphere, and phylloaphere microbes mainly came from rhizosphere. FAPROTAX function prediction showed that indicator species sensitive to intercropping and crop rotation were involved in nitrogen/phosphorus cycle and degradation process, respectively. In addition, compared to the continuous cropping, intercropping increased the stochastic assembly processes of bacterial communities in plant-associated compartments, while crop rotation increased the complexity and stability of the rhizosphere network and the deterministic assembly process. Our study highlights the importance of intercropping and crop rotation, as well as rhizosphere and phyllosphere compartments for future crop management and sustainable agricultural regulation of crop microbial communities.

Linking Bacterial-Fungal Relationships to Microbial Diversity and Soil Nutrient Cycling.

Biodiversity is important for supporting ecosystem functioning. To evaluate the factors contributing to the strength of microbial diversity-function relationships in complex terrestrial ecosystems, we conducted a soil survey over different habitats, including an agricultural field, forest, wetland, grassland, and desert. Soil microbial multidiversity was estimated by the combination of bacterial and fungal diversity. Soil ecosystem functions were evaluated using a multinutrient cycling index (MNC) in relation to carbon, nitrate, phosphorus, and potassium cycling. Significant positive relationships between soil multidiversity and multinutrient cycling were observed in all habitats, except the grassland and desert. Specifically, community compositions showed stronger correlations with multinutrient cycling than α-diversity, indicating the crucial role of microbial community composition differences on soil nutrient cycling. Importantly, we revealed that changes in both the neutral processes (Sloan neutral modeling) and the proportion of negative bacterial-fungal associations were linked to the magnitude and direction of the diversity-MNC relationships. The habitats less governed by neutral processes and dominated by negative bacterial-fungal associations exhibited stronger negative microbial α-diversity-MNC relationships. Our findings suggested that the balance between positive and negative bacterial-fungal associations was connected to the link between soil biodiversity and ecosystem function in complex terrestrial ecosystems. This study elucidates the potential factors influencing diversity-function relationships, thereby enabling future studies to forecast the effects of belowground biodiversity on ecosystem function.IMPORTANCE The relationships between soil biodiversity and ecosystem functions are an important yet poorly understood topic in microbial ecology. This study presents an exploratory effort to gain predictive understanding of the factors driving the relationships between microbial diversity and potential soil nutrient cycling in complex terrestrial ecosystems. Our structural equation modeling and random forest analysis revealed that the balance between positive and negative bacterial-fungal associations was clearly linked to the strength of the relationships between soil microbial diversity and multiple nutrients cycling across different habitats. This study revealed the potential factors underpinning diversity-function relationships in terrestrial ecosystems and thus helps us to manage soil microbial communities for better provisioning of key ecosystem services.

Soil bacterial diversity correlates with precipitation and soil pH in long-term maize cropping systems.

Unraveling the key drivers of bacterial community assembly in agricultural soils is pivotal for soil nutrient management and crop productivity. Presently, the drivers of microbial community structure remain unexplored in maize cropping systems under complex and variable environmental scenarios across large spatial scales. In this study, we conducted high-throughput 16S rRNA gene sequencing and network analysis to identify the major environmental factors driving bacterial community diversity and co-occurrence patterns in 21 maize field soils across China. The results show that mean annual precipitation and soil pH are the major environmental factors that shape soil bacterial communities in maize soils. The similarities of bacterial communities significantly decreased with increasing geographic distance between different sites. The differences in spatial turnover rates across bacterial phyla indicate the distinct dispersal capabilities of bacterial groups, and some abundant phyla exhibited high dispersal capabilities. Aeromicrobium, Friedmanniella, Saccharothrix, Lamia, Rhodococcus, Skermanella, and Pedobacter were identified as keystone taxa. Based on the node-level and network-level topological features, members of the core microbiome were more frequently found in the center of the ecosystem network compared with other taxa. This study highlights the major environmental factors driving bacterial community assembly in agro-ecosystems and the central ecological role of the core microbiome in maintaining the web of complex bacterial interactions.