Global climate gradients structure soil Legionella diversity, relative abundance and pathogen distributions

Legionnaires disease has increased sixfold since 2000 in the United States, yet environmental reservoirs such as soils remain understudied sources of infection. It remains unclear how the diversity and abundance of environmental pathogens, such as Legionella, will shift as the climate continues to change. Here, we utilize 4,287 publicly available global soil 16S rRNA gene amplicon datasets to analyze how the distribution of the genus Legionella, including pathogenic lineages, varies across continental-scale biogeographic regions and along climatic and geochemical gradients. Legionella relative abundance increased across the joint precipitation-air temperature gradient, and mixed-effects modeling indicated that the chance of detecting Legionella in soils increased substantially when annual precipitation reached [~]500 mm. Legionella diversity was characterized by high spatial turnover, with the majority of abundant ASVs restricted to individual regions despite broad phylogenetic representation across the genus. Further, fewer than 2% of our 16S-derived Legionella sequences matched ASVs corresponding to characterized species, and the clinically dominant species L. pneumophila was rarely detected. In contrast, ASVs matching several other known pathogens (L. longbeachae, L. anisa, L. bozemanae, L. cincinnatiensis) were orders of magnitude more common than L. pneumophila in soils. Moreover, pathogenic Legionella ASVs were detected significantly more frequently at warmer and wetter conditions. Collectively, our findings suggest that Legionella relative abundance and diversity in soils, especially pathogenic lineages, are shaped by both dispersal and climatic filtering. As temperature and precipitation regimes shift in the future, our results imply that soils should be an important pathogen source to monitor and that Legionella species beyond L. pneumophila warrant increased ecological and public health attention.