Soil-Nutrient Depletion and Microbial Community Restructuring in Continuous Celery Cropping: Opposing Responses of Bacteria and Fungi

Continuous cropping obstacles represent a major constraint in agricultural production, yet the underlying microbial mechanisms remain incompletely understood. This study systematically compared soil physicochemical properties, microbial diversity, community composition, and nutrient-microbe relationships between continuous cropping (CC) and non-continuous cropping (CK) celery rhizospheres using high-throughput sequencing, soil physicochemical analysis, and Mantel tests. The results revealed that CC soils exhibited severe depletion of available potassium (AK, 69.9% decreased) and alkali-hydrolyzable nitrogen (AN, 65.9% decreased), accompanied by a modest but statistically significant accumulation of total phosphorus (TP, 8.0% increased). Strikingly, bacterial and fungal communities displayed diametrically opposed diversity responses: CC significantly reduced bacterial α-diversity (Shannon: 5.66 vs. 6.67, p < 0.01) and richness (ACE: 2018 vs. 2623, p < 0.01), whereas fungal diversity and richness more than doubled under CC (ACE: 619 vs. 296, p < 0.01; Shannon: 4.13 vs. 3.34, p < 0.01). β-diversity analyses (NMDS and ANOSIM) confirmed fundamental community restructuring in CC soils for both microbial domains. At the taxonomic level, CC soils showed significant depletion of beneficial plant growth-promoting rhizobacteria (PGPR), including Bacillus (↓89.3%), Mesobacillus (↓72.8%), and Pseudomonas (↓30.8%), coupled with dramatic enrichment of the phytopathogenic genus Fusarium (10.9-fold increase, 8.81% vs. 0.81%, p < 0.001). LEfSe analysis identified Fusarium, Arrhenia, and Mortierella as specific biomarkers of CC soils, whereas Bacillus, Mesobacillus, Cladosporium, and Alternaria were biomarkers of CK soils. Mantel tests further revealed that CC significantly altered nutrient-microbe coupling relationships, with bacterial communities significantly correlated with TP, AN, and OC, and fungal communities with TP, TK, AP, and AN. Collectively, these findings demonstrate that continuous celery cropping shifts the rhizosphere microbiome from a bacterial-dominated profile associated with beneficial taxa (e.g., Bacillus, Pseudomonas) toward a fungal-enriched profile dominated by the pathogen Fusarium, suggesting a potential transition from a putatively disease-suppressive to a disease-conducive microbial state.