Metagenomic characterization of the metabolism, evolution, and global distribution of Candidatus Accumulibacter members in wastewater treatment plants

TL;DR

This study explores the global diversity and evolution of Candidatus Accumulibacter in wastewater treatment plants, revealing new genetic and metabolic adaptations that support their ecological roles.

Contribution

The discovery of a new clade and insights into genome plasticity and metabolic adaptation in Candidatus Accumulibacter.

Findings

A new clade (Clade IV) of Candidatus Accumulibacter was identified, expanding known phylogenetic diversity.

Genome analyses revealed clade-specific gene gain and loss, particularly in nitrogen metabolism, indicating divergent evolutionary paths.

Metabolic modeling and experimental validation showed amino acid autotrophy and distinct carbon utilization strategies.

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 into understanding how microbial communities adapt and respond under engineered environmental conditions.

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