Physiological adaptations of a minimal bacterial consortium enable robust ammonia oxidation at extremely acidic pH

Microbial communities can efficiently mediate aerobic ammonia oxidation even at acidic pH. However, little is known about the strategies that enable them to simultaneously mitigate acidic and nitrosative stresses. Here, we integrate genome-resolved meta-omic analyses with chemical measurements to infer the composition, metabolic exchange, and stress adaptations of microbial consortia in three acidic nitrification bioreactors operated between pH 2.0 and 5.0. At pH 5.0, the dominant ammonia-oxidising bacterium (AOB) across all conditions was a novel Nitrosococcaceae species, designated "Candidatus Nitrosoglobus kelleri." It reached a relative abundance of up to 56% and possessed genes for ammonia oxidation, aerobic respiration, and carbon fixation. At pH 2.0, the community was strongly simplified and dominated by "Ca. Nitrosoglobus kelleri" together with Mycobacterium species; genome-resolved and transcriptional evidence suggested potential metabolic linkages related to carbon and nitrogen compound cycling. Both "Ca. Nitrosoglobus kelleri" and Mycobacterium spp. concurrently activate metabolic mechanisms to maintain intracellular pH homeostasis, detoxify reactive nitrogen species, and reinforce their cellular envelopes. Despite inhabiting aerobic bioreactors, consortia members also expressed denitrification genes at high levels, likely to eliminate reactive nitrogen species such as nitrite and nitric oxide produced during incomplete nitrification, with a trade-off in respiratory efficiency. Collectively, these findings provide critical insights into the metabolic adaptations of minimalistic microbial communities at extremely low pH. In addition to enhancing understanding of microbial nitrogen cycling, this work has potential implications for improving wastewater treatment technologies through acidic nitrification processes.