Plant Diversity Induces Shifts from Microbial Generalists to Specialist by Enhancing Niche Differentiation, Microbiome Connectivity, and Network Stability in a Temperate Grassland

Soil microbiota are key players of terrestrial ecosystem functioning, including decomposition, soil organic matter formation, and nutrient cycling, and interact strongly with plants in the rhizosphere. Several studies have demonstrated the potential of plants to alter soil microbiome assembly and functioning (i.e., through manipulation of soil organic matter pools via root exudation), which can be critical for sustaining soil ecosystem functioning. Using soil from a long-term biodiversity experiment in Germany, we investigated how soil microbial communities responded to variations in plant species richness (1–16 species), functional group richness (1–4 groups), and plant identity (grasses, legumes, small herbs, and tall herbs) using 16S rRNA gene and ITS amplicon sequencing. We examined bacterial and fungal community structure, metabolic potential, and microbial network architecture to better understand the role of the soil microbiome and its net positive relationship between biodiversity and ecosystem functioning. Plant diversity induced gradual shifts in microbial community composition, while increasing soil organic carbon and nitrogen stocks. Microbial networks exhibited increased connectivity, particularly between bacteria and fungi. Meanwhile, mutualistic and antagonistic functional guild representation increased, that is the sum total of plant-beneficial (i.e., endophytes) and plant- or fungi-detrimental (i.e., pathogens and parasites) fungal guilds, respectively. Key nodes shifted from generalist taxa at low plant diversity to more specialized communities at high plant diversity. Notably, fungi responded more strongly than bacteria, and their functional potential was driven by plant functional identity rather than species richness. At low plant diversity, generalist taxa likely exploit less complex and diverse organic carbon inputs, allowing them to dominate available niches. In contrast, higher plant diversity promotes a broader array of specialist taxa that likely benefit from the greater diversity of organic carbon compounds, and thus greater niche availability. As network complexity grows, ecosystem functions are being distributed across more taxa, leading to greater microbiome stability, and ultimately more efficient soil carbon and nutrient cycling. Our findings suggest that higher plant diversity strengthens microbial functioning and enhances microbiome resilience, that is the capacity of the microbial community to maintain soil functioning despite environmental disturbances.