An ecological-evolutionary perspective on the genomic diversity and habitat preferences of the Acidobacteriota

Members of the phylum Acidobacteriota inhabit a wide range of ecosystems including soils. We analysed the global patterns of distribution and habitat preferences of various Acidobacteriota lineages across major ecosystems (soil, engineered, host-associated, marine, non-marine saline and alkaline and terrestrial non-soil ecosystems) in 248 559 publicly available metagenomic datasets. Classes Terriglobia, Vicinamibacteria, Blastocatellia and Thermoanaerobaculia were highly ubiquitous and showed a clear preference to soil over non-soil habitats, while classes Aminicenantia and Holophagae showed preferences to non-soil habitats. However, while specific preferences were observed, most Acidobacteriota lineages were habitat generalists rather than specialists, with genomic and/or metagenomic fragments recovered from soil and non-soil habitats at various levels of taxonomic resolution. Comparative analysis of 1930 genomes strongly indicates that phylogenetic affiliation plays a more important role than the habitat from which the genome was recovered in shaping the genomic characteristics and metabolic capacities of the Acidobacteriota. The observed lack of strong habitat specialization and habitat-transition-driven lineage evolution in the Acidobacteriota suggest ready cross-colonization between soil and non-soil habitats. We posit that such capacity is key to the successful establishment of Acidobacteriota as a major component in soil microbiomes post-ecosystem disturbance events or during pedogenesis.