Motile and non-motile Listeria species adopt distinct genomic and ecological strategies to achieve broad geographic ranges in soil

Abstract Broad geographic ranges indicate high ecological versatility and are generally associated with low extinction risk. Motility is not only a physiological feature, but also a core ecological trait for bacteria. However, the genomic foundations underlying the broad geographic ranges of motile and non-motile bacteria remain poorly understood. To address this, we analyzed 141 and 90 genomes of Listeria welshimeri and L. booriae , systematically screened from 1,004 soil samples across the United States, representing widespread motile and non-motile species, respectively. We show that L. welshimeri exhibits restricted phylogeographic structure and a weak distance-decay relationship, suggesting minimal geographic barriers to dispersal. Its high dispersal capacity likely stems from enhanced motility and effective host colonization, evidenced by strong positive selection on flagellar genes and the close relatedness to isolates from wild birds. In contrast, L. booriae displays a regionally endemic distribution and limited dispersal. With a large, open pangenome, L. booriae appears strongly adapted to local environments. This is evidenced by pronounced positive selection on genes involved in inorganic ion, amino acid, and coenzyme transport and metabolism, as well as strong associations with abiotic factors, particularly climate, and accompanying bacterial consortia. In summary, to establish widespread distributions, L. welshimeri tends to rely on movement and colonization of wildlife hosts to facilitate long-distance dispersal, while L. booriae leverages genomic plasticity and metabolic versatility that enable adaptation to diverse environmental conditions. These findings highlight the distinct genomic foundations and ecological strategies that motile and non-motile bacteria use to achieve broad geographic ranges in the environment.