Trait-based divergence in free-living and particle-attached bacterial succession during algal biomass degradation

Phytoplankton blooms are increasingly influenced by climate change and eutrophication, profoundly affecting coastal carbon dynamics and microbial succession. Understanding how microbial communities respond to bloom degradation is critical for predicting ecosystem feedbacks to environmental change. Here, we performed in situ microcosm experiments with three bloom-forming species and combined physicochemical and biological analyses to investigate the successional dynamics of free-living (FL) and particle-attached (PA) bacteria. Organic carbon degradation was resolved into three phases (I-III), each characterized by shifts among abundant, intermediate, and rare groups. Both FL and PA communities underwent transitions from r-to K-strategists, primarily driven by carbon depletion but mediated by contrasting mechanisms: FL succession was stochastic and supported by rare taxa as a functional seed bank, while PA restructuring followed deterministic selection. Network analysis revealed divergent adaptive strategies, with FL communities maintained high connectivity through rare taxa, conferring functional redundancy and stability, whereas PA communities displayed increasing modularity with delayed adaptation buffered by particulate nutrient availability. Keystone taxa exhibited clear phase-dependent turnover, with FL shifting from Tenacibaculum and Owenweeksia to Chitinophagales and Erythrobacter, and PA from Enterobacterales to Bradymonadales, and then to Chitinophagales, Rhodopirellula, and Verrucomicrobiale. Trait dynamics further indicated a progression from motility and sensing functions toward nutrient acquisition, energy conservation and stress tolerance. Collectively, our findings highlight the ecological strategies underpinning microbial resilience to bloom collapse, providing new insights into how coastal ecosystems may respond to ongoing climate-driven changes in bloom dynamics and organic matter cycling.