Local Fungi Promote Plant Growth by Positively Affecting Rhizosphere Metabolites to Drive Beneficial Microbial Assembly

Ecological restoration in the cold and high-altitude mining areas of the Qinghai-Tibet Plateau is faced with dual challenges of extreme environments and insufficient microbial adaptability. This study aimed to screen local microbial resources with both extreme environmental adaptability and plant-growth-promoting functions. Local fungi (DK; F18-3) and commercially available bacteria (B0) were used as materials to explore their regulatory mechanisms for plant growth, soil physicochemical factors, microbial communities, and metabolic profiles in the field. Compared to bacterial treatments, local fungi treatments exhibited stronger ecological restoration efficacy. In addition, the DK and F18-3 strains, respectively, increased shoot and root biomass by 23.43% and 195.58% and significantly enhanced soil nutrient content and enzyme activity. Microbiome analysis further implied that, compared with the CK, DK treatment could significantly improve the α-diversity of fungi in the rhizosphere soil (the Shannon index increased by 14.27%) and increased the amount of unique bacterial genera in the rhizosphere soil of plants, totaling fourteen genera. Meanwhile, this aggregated the most biomarkers and beneficial microorganisms and strengthened the interactions among beneficial microorganisms. After DK treatment, twenty of the positively accumulated differential metabolites (DMs) in the plant rhizosphere were highly positively associated with six plant traits such as shoot length and root length, as well as beneficial microorganisms (e.g., <i>Apodus</i> and <i>Pseudogymnoascus</i>), but two DMs were highly negatively related to plant pathogenic fungi (including <i>Cistella</i> and <i>Alternaria</i>). Specifically, DK mainly inhibited the growth of pathogenic fungi through regulating the accumulation of D-(+)-Malic acid and Gamma-Aminobutyric acid (<i>Cistella</i> and <i>Alternaria</i> decreased by 84.20% and 58.53%, respectively). In contrast, the F18-3 strain mainly exerted its antibacterial effect by enriching <i>Acidovorax</i> genus microorganisms. This study verified the core role of local fungi in the restoration of mining areas in the Qinghai-Tibet Plateau and provided a new direction for the development of microbial agents for ecological restoration in the Qinghai-Tibet Plateau.