Acinetobacter baumannii’s lifestyle includes soil-dwelling colonization of decaying plant material and airborne spread

Acinetobacter baumannii is a Gram-negative nosocomial pathogen that is notorious for its rapid development of antibiotic resistance. However, its ecology and evolution outside hospital settings remain poorly defined. Here, we demonstrate that the natural lifestyle of A. baumannii includes soil-dwelling and airborne dissemination, which helps explaining its adaptability and tolerance to desiccation, radiation and antibiotics, and thus its predisposition to establish within hospitals. Starting from white stork nestlings previously discovered as a reservoir, we studied food chains and associated environments and identified soil and decaying plants as habitats. We demonstrate that sterilized plant material is rapidly colonized by airborne A. baumannii. A set of 401 genomes were sequenced and compared to publicly available genomes, revealing numerous links between wildlife isolates and hospital strains, and disclosing intercontinental dispersal. Our pan-genome estimate of the species (~51,000 gene families) more than doubles that of previous studies. Our data further suggest massive radiation of the species early after its emergence, possibly fostered by human activity since the Neolithic. Now, it is possible to study the ecology and evolution of A. baumannii in nature at an unprecedented temporal and spatial resolution and to elucidate the adaptive evolution of environmental bacteria towards multidrug-resistant opportunistic pathogens.