Trait-based frameworks, notably Grime's competitor–stress-tolerant–ruderal theory, offer a powerful lens for predicting how environmental fluctuations govern community structure. Yet, classical ecological models assume environments combining extreme stress and intense disturbance are non-viable for sustained colonisation, leaving a critical bottleneck in our ability to predict how microbial systems withstand compounded operational pressures. This gap severely hinders the predictive management of engineered microbiomes critical for global waste-to-energy conversion. Here we extend the application of classic ecological frameworks by demonstrating that anaerobic digester microbiomes deploy distinct, predictable life-history strategies across a 182-day compounded gradient of biomass turnover and organic loading. High-intensity single-event disturbances drive severe volatile fatty acid accumulation (propionate reaching 2,955 mg L⁻¹), selectively shifting the microbiome toward stress-tolerant and stress-tolerant–ruderal strategies. Traits associated with ribosome function, molecular chaperones, and enzymatic reactive oxygen species detoxification were particularly enriched under highly disturbed conditions. Conversely, intermediate regimes were associated with ruderal strategies that prioritise rapid growth over resource-uptake efficiency, dropping total chemical oxygen demand removal to 41%. Cross-system comparisons encompassing anaerobic digestion, activated sludge, and soil ecosystems, revealed both universal and context-dependent ecological traits. Survival-associated traits linked to cell maintenance and repair, protective mechanisms, and cell motility were universally associated with stress-tolerant or ruderal strategies across ecosystems, whereas nutrient transport and metabolic traits exhibited greater context dependency. These insights establish a gene-resolved framework that reconciles microbial trait selection with ecological theory, providing a roadmap to engineer microbiome resilience against process failures.

Candidatus Accumulibacter, a prominent polyphosphate-accumulating organism (PAO) in wastewater treatment, plays a crucial role in enhanced biological phosphorus removal (EBPR). The genetic underpinnings of its polyphosphate accumulation capabilities, however, remain largely unknown. Here, we conducted a comprehensive genomic analysis of Ca. Accumulibacter-PAOs and their relatives within the Rhodocyclaceae family, identifying 124 core genes acquired via horizontal gene transfer (HGT) at its least common ancestor. Metatranscriptomic analysis of an enrichment culture of Ca. Accumulibacter revealed active transcription of 44 of these genes during an EBPR cycle, notably including the polyphosphate kinase 2 (PPK2) gene instead of the commonly recognized polyphosphate kinase 1 (PPK1) gene. Intriguingly, the phosphate regulon (Pho) genes showed minimal transcriptions, pointing to a distinctive fact of Pho dysregulation, where PhoU, the phosphate signaling complex protein, was not regulating the high-affinity phosphate transport (Pst) system, resulting in continuous phosphate uptake. To prevent phosphate toxicity, Ca. Accumulibacter utilized the laterally acquired PPK2 to condense phosphate into polyphosphate, resulting in the polyphosphate-accumulating feature. This study provides novel insights into the evolutionary emergence of the polyphosphate-accumulating trait in Ca. Accumulibacter, offering potential advancements in understanding the PAO phenotype in the EBPR process.