Plant Diversity and Fungal Richness Regulate the Changes in Soil Multifunctionality in a Semi-Arid Grassland

SIMPLE SUMMARY: Understanding relationships between biodiversity and ecosystem functions is important in the context of global plant diversity loss. We evaluated the relationships between soil bacterial and fungal diversity, rare microbial taxa, and soil multifunctionality in a semi-arid grassland with varied plant diversity levels. The fungal richness rather than bacterial richness was positively related to soil multifunctionality. The relative abundance of saprotrophs was positively correlated with soil multifunctionality, and the relative abundance of pathogens was negatively correlated with soil multifunctionality. Furthermore, the rare fungal taxa played a disproportionate role in regulating soil multifunctionality. The shift of plant biomass allocation patterns increased plant below-ground biomass in the high diversity plant assemblages, which can alleviate soil microbial carbon limitations and enhance the fungal richness, thus promoting soil multifunctionality. This study provides a new perspective for evaluating the relative roles of fungal and bacterial diversity in maintaining multiple soil functions under global plant diversity loss scenarios. ABSTRACT: Loss in plant diversity is expected to impact biodiversity and ecosystem functioning (BEF) in terrestrial ecosystems. Soil microbes play essential roles in regulating ecosystem functions. However, the important roles and differences in bacterial and fungal diversity and rare microbial taxa in driving soil multifunctionality based on plant diversity remain poorly understood in grassland ecosystems. Here, we carried out an experiment in six study sites with varied plant diversity levels to evaluate the relationships between soil bacterial and fungal diversity, rare taxa, and soil multifunctionality in a semi-arid grassland. We used Illumina HiSeq sequencing to determine soil bacterial and fungal diversity and evaluated soil functions associated with the nutrient cycle. We found that high diversity plant assemblages had a higher ratio of below-ground biomass to above-ground biomass, soil multifunctionality, and lower microbial carbon limitation than those with low diversity. Moreover, the fungal richness was negatively and significantly associated with microbial carbon limitations. The fungal richness was positively related to soil multifunctionality, but the bacterial richness was not. We also found that the relative abundance of saprotrophs was positively correlated with soil multifunctionality, and the relative abundance of pathogens was negatively correlated with soil multifunctionality. In addition, the rare fungal taxa played a disproportionate role in regulating soil multifunctionality. Structural equation modeling showed that the shift of plant biomass allocation patterns increased plant below-ground biomass in the highly diverse plant plots, which can alleviate soil microbial carbon limitations and enhance the fungal richness, thus promoting soil multifunctionality. Overall, these findings expand our comprehensive understanding of the critical role of soil fungal diversity and rare taxa in regulating soil multifunctionality under global plant diversity loss scenarios.