A respiro-fermentative strategy to survive nanoxia in Acidobacterium capsulatum

Microbial soil habitats are characterized by rapid shifts in substrate and nutrient availabilities, as well as chemical and physical parameters. One such parameter that can vary in soil is oxygen; thus, microbial survival is dependent on adaptation to this substrate. To better understand the metabolic abilities and adaptive strategies to oxygen-deprived environments, we combined genomics with transcriptomics of a model organism, Acidobacterium capsulatum, to explore the effect of decreasing, environmentally relevant oxygen concentrations. The decrease from 10 to 0.1 µM oxygen (3.6 to 0.036 pO2% present atmospheric level, respectively) caused the upregulation of the transcription of genes involved in signal transduction mechanisms, energy production and conversion and secondary metabolites biosynthesis, transport, and catabolism based on clusters of orthologous group categories. Contrary to established observations for aerobic metabolism, key genes in oxidative stress response were significantly upregulated at lower oxygen concentrations, presumably due to an NADH/NAD+ redox ratio imbalance as the cells transitioned into nanoxia. Furthermore, A. capsulatum adapted to nanoxia by inducing a respiro-fermentative metabolism and rerouting fluxes of its central carbon and energy pathways to adapt to high NADH/NAD+ redox ratios. Our results reveal physiological features and metabolic capabilities that allowed A. capsulatum to adapt to oxygen-limited conditions, which could expand into other environmentally relevant soil strains.