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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.

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.

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.

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.

Protists are essential for nutrient cycling and plant performance in diverse ecosystems. However, the biogeographic patterns and driving forces (i.e. abiotic or biotic factors) of protistan communities remain poorly understood in agricultural ecosystems. Here, the biogeographic patterns of soil protists were assessed in adjacent pairs of maize and rice fields across eastern China. By combining our results with previously published datasets, we presented the first evidence that the α- and β-diversity of protists were highly structured by bacterial diversity in maize soils and fungal diversity in rice soils, respectively. Consistently, network analyses showed higher connectedness of protists to bacteria in maize soils, but higher connectedness of protists to fungi in rice soils. In addition, bacteria were more correlated with protistan consumers in maize soils, whereas fungi were more associated with protistan phototrophs. Protists in rice soils with lower diversity displayed broader environmental breadth and stronger phylogenetic conservatism than those in maize soils. Taken together, our results provides novel insights into the importance of biotic factors (trophic interrelationships) in driving the biogeographic patterns of soil protistan community in distinct agricultural ecosystems.