Zhaojuan Zhang, Jing Zhao, Jiaxin Li, Jialing Jin, Zhuang Li, Xin Li, Changqi Zhu, Steven L Stephenson, Yu Li, Pu Liu
The intensive cultivation of black soils severely threatens the structural stability of the agricultural ecosystems in which they occur. While the compositional responses of bacteria and fungi to such degradation are well-documented, the eco-evolutionary fate of protistan apex predators, crucial regulators of the microbial carbon loop, remains a critical blind spot. Herein, we integrate large-scale molecular phylogenetics, high-resolution morphological phenotyping, and multi-kingdom amplicon sequencing to decode the assembly and trophic dynamics of social amoebae across a tillage chronosequence. We uncovered previously unrecognized phylogenetic diversity of dictyostelids persisting despite apparent macro-ecological resilience. However, this resilience masks a marked compression of vertical spatial stratification-mechanical tillage erodes vertical spatial niches and imposes severe morphological filtering, consistently depleting large, migratory species while selecting for structurally robust, allometrically constrained phenotypes. Crucially, we identified a pH-driven pathway associated with predator-prey decoupling. Progressive soil acidification coincides with a macro-ecological pattern where dictyostelid diversity uncouples from bulk bacterivory and scales selectively with Gram-negative bacteria prey, representing a testable hypothesis for future grazing assays. Furthermore, this study revealed structural dependencies on specific saprotrophic fungi, and we have proposed an empirical hypothesis that amoebae may utilize mycelial networks as physical scaffolding ("micro-highways") to compensate for the tillage-induced loss of physical soil pores, a ecological model that warrants future microscopic validation. These findings provide a foundational framework for understanding soil ecology, demonstrating that agricultural disturbance does not merely homogenize communities but is associated with micro-food web reorganization through cryptic phenotypic trade-offs, potentially altering the biogeochemical functionality of degraded soils.