Dark CO2 Fixation via the Ethylmalonyl-CoA Pathway Establishes Metabolic Parity: A Stoichiometric Basis for Compounding Ecosystem Shifts

In microbial ecosystems, the coexistence of competing microbial groups has long puzzled researchers. While many heterotrophs accumulate polyphosphate to manage energy and redox balance, certain lineages lack this ability yet maintain similar intracellular redox states. To explore this phenomenon, researchers employed enhanced biological phosphorus removal in a macrocosm, combining stoichiometry with metaproteomics to identify alternative metabolic strategies.

They discovered that glyceroglycogen-accumulating organisms (GAOs) can achieve metabolic parity with polyphosphate-accumulating organisms (PAOs) through a unique redox-buffering mechanism: the re-assimilation of CO2/HCO3- via the ethylmalonyl-CoA pathway. This inorganic carbon fixation not only conserves structural carbon but also tightly regulates redox states, eliminating the presumed bioenergetic disadvantage of GAOs.

GAOs further bolster their bioenergetic efficiency through energy-efficient high-affinity acetate activation, ferredoxin-centered biochemistry, and neutral polyhydroxyalkanoates (PHA) mobilization. Surprisingly, the addition of formate disrupted this PAO/GAO balance, creating an asymmetric bioenergetic niche favoring GAOs. Stoichiometric simulations demonstrated that this formate supplementation grants GAOs a per-cycle energy advantage.

By controlling solids retention time without impacting hydraulic throughput, cells with intracellular inventory maintain dominance, translating marginal per-cycle advantages into a generational edge and leading to a rapid community shift from co-dominance to GAO dominance. This study highlights the importance of resource management and generational metabolic compounding in shaping microbial community assembly, challenging traditional steady-state models that assume single-substrate and single-cycle conditions.