Urbanization destabilizes rhizosphere multitrophic networks with cascading risks to urban One Health

How urbanization reshapes rhizosphere health, trophic cascades, and ecosystem multifunctionality (EMF) across municipal green infrastructures remains unresolved. Herein, we integrated soil physicochemical profiling, heavy metal toxicological risk modeling, ecoenzymatics, and tri-kingdom sequencing across a cold-temperate Mollisol metropolitan network (n = 144) spanning four urbanization tiers, seasons, and vegetation types. Urbanization selectively decoupled subterranean biogeochemistry: severe cadmium accumulation and ecological hazards (RI > 150) were confined to urban cores, whereas macronutrient pools and metabolic constraints (persistent C- and predominant N-limitation, Vector A < 45°) followed seasonal rhythms, preserving non-carcinogenic safety (HI < 1.0). Multitrophic community differentiation was governed by taxon replacement (> 70%–85%) and stochastic drift (48.0%–71.5%, neutral R² = 0.38–0.62). Protists exhibited the broadest environmental tolerances [ln(tolerance + 1): 0.27–0.36] whereas fungi showed the highest species-level niche breadth (P < 0.05), with trait adaptability evolutionarily decoupled from phylogenetic conservatism in fungi and protists (P > 0.05). Concurrently, urbanization collapsed cross-trophic network robustness (natural connectivity dropping from 0.81 to 0.33) and escalated negative competitive interactions to 47.9%. Challenging monotonic biodiversity–functioning paradigms, rhizosphere EMF peaked at an empirical trophic optimum of 1.64 (Protists/[Bacteria + Fungi]). Safe operating space (SOS) modeling confirmed that geochemical toxicity (I_Metal) constrained biological vitality (I_Biol), impairing protist-depleted communities. Cascading through Cornell Soil Health Assessment (CASH) matrices, the framework established herein provides an empirical bio-regulation blueprint bridging microscale rhizosphere vitality with macroscale urban One Health governance.