Nonlinear response mechanisms of microbial communities to coral reef biogeomorphy in the South China Sea.

To resolve how planktonic microbial composition, assembly mechanisms, and interaction architectures vary across coral reef biogeomorphic states, we sought to identify process-relevant indicators of reef resilience. We analyzed size-fractionated microbiomes from 57 stations in the South China Sea using 16S/18S rRNA amplicon sequencing. A distance-decay model defined a near-coral reef influence zone within 588 m, and reefs were classified into Poor, Moderate, and Good states based on coral density metrics. Results showed that microbial composition diverged significantly between near-coral reefs and off-coral reef zones. Although alpha diversity remained relatively stable, characteristic coral reef amplicon sequence variants (ASVs) showed clear state-associated variation across reef biogeomorphic states. The assembly of coral reef characteristic ASVs was predominantly stochastic, yet deterministic processes strengthened under intermediate conditions, indicating a transitional restructuring phase. Network complexity displayed a hump-shaped pattern, peaking in moderate states, whereas networks in good-condition reefs were sparser but more stable due to cross-kingdom interactions and increased module hubs. Ultimately, embedding microbiome analyses within a biogeomorphic framework reveals nonlinear, state-dependent microbial reorganization missed by standard richness metrics. These responsive taxa and interaction architectures jointly provide mechanistic indicators for diagnosing coral reef health in rapidly changing tropical seas. IMPORTANCE: Microbial composition, assembly processes, and interaction architecture jointly provide process-relevant indicators of reef condition and resilience across coral-reef biogeomorphic states. Although alpha diversity remained broadly stable across space and biogeomorphic grades, substantial microbial turnover, pronounced state responsiveness of characteristic taxa, and marked shifts in network organization revealed strong state dependence in microbial reorganization. Responsive taxa and interaction-architecture metrics jointly provide mechanistic, process-relevant indicators for diagnosing reef condition and resilience in rapidly changing tropical seas.