Genome-reduced Aridivitia evolved predation to thrive in Earth’s oligotrophic depths

Abstract Deep soils represent one of Earth’s largest yet most enigmatic microbial habitats, where survival strategies under extreme oligotrophy remain poorly understood. Here, we report the Aridivitia group, a globally distributed bacterial lineage enriched in oligotrophic soils and thriving down to 22 m depth across sites in the United States and China. Despite its genome reduction (average size ~2.9 Mb), Aridivitia exhibits high metabolic flexibility in utilizing diverse carbon and energy sources. Cellular, genomic, and metatranscriptomic evidence, including small cell and genome sizes, host-associated metabolism, and the active expression of attachment- and attack-associated surface structures such as Tad pili and pore-forming toxins, indicate a predatory lifestyle in Aridivitia. Ancestral genome reconstruction reveals that Aridivitia originated as free-living mixotrophs, but subsequently lost the ability to fix carbon as they evolved a predatory lifestyle. Collectively, Aridivitia exemplifies a unique evolutionary strategy that reconciles genome reduction with functional versatility, expanding our understanding of microbial adaptation and evolution at the energetic limits of life.