Abstract
Deciphering the genomic basis of ecological diversification in activated sludge microbiomes is essential for optimizing treatment technology and advancing microbial ecology. Here, we present a global genome-resolved investigation of Candidatus Accumulibacter, the primary functional agent of enhanced biological phosphorus removal, based on 828 metagenomes from wastewater treatment plants across six continents. We recovered 104 high-quality Candidatus Accumulibacter metagenome-assembled genomes, discovering a new clade (Clade IV), substantially expanding the known phylogenetic diversity and revealing a ubiquitous yet geographically heterogeneous global distribution. Phylogenomic and pangenome analyses uncovered extensive clade-specific gene gain and loss, particularly in nitrogen metabolism, suggesting divergent evolutionary trajectories shaped by relaxed selection and niche adaptation. Genome-wide patterns of convergent streamlining and enriched antiviral defense systems indicate selective pressures from strong competition and viral predation. Constraint-based metabolic modeling revealed pervasive amino acid autotrophies and metabolic complementarity, coupled with distinct carbon utilization strategies that support ecological specialization across operational settings. Experimental validation reconciled model-phenotype discrepancies, highlighting the importance of transporter promiscuity and gene regulation in carbon substrate assimilation. Collectively, our findings redefine Candidatus Accumulibacter as a dynamic model of microbial genome plasticity, metabolic adaptation, and ecological resilience, providing an insight for understanding how microbial communities adapt and respond under engineered environmental conditions.