Members of the phylum Acidobacteria are abundant and ubiquitous across soils. We performed the largest (to date) comparative genome analysis spanning subdivisions 1, 3, 4, 6, 8, and 23 (n=24) with the goal to identify features to help explain their prevalence in soils and understand their ecophysiology. In contrast to earlier studies, our analysis revealed that bacteriophage integration events along with transposable and mobile elements influenced the structure and plasticity of these genomes. Low- and high-affinity respiratory oxygen reductases were detected in multiple genomes, suggesting the capacity for growing across different oxygen gradients. Amongst many genomes, the capacity to use a diverse collection of carbohydrates, as well as inorganic and organic N sources (such as extracellular peptidases), were detected - both advantageous traits in environments with fluctuating nutrient environments. We also identified multiple soil acidobacteria with the potential to scavenge atmospheric concentrations of H2 , now encompassing mesophilic soil strains within the subdivision 1 and 3, in addition to a previously identified thermophilic strain in subdivision 4. This large-scale acidobacteria genome analysis reveals traits that provide genomic, physiological and metabolic versatility, presumably allowing flexibility and versatility in the challenging and fluctuating soil environment. This article is protected by copyright. All rights reserved.