Expansion, restructuring and characterization of the Legionellaceae family

Legionellaceae are a large and widespread family of facultative intracellular bacteria with high clinical relevance. While Legionella pneumophila , the most clinically relevant species, is relatively well studied, very limited information is available regarding the other species belonging to this family. Here, we analysed all publicly-available Legionellaceae genomes and metagenomic-assembled genomes, nearly doubling the number of recognized species in this family and finding evidence for the need to restructure the family’s taxonomy including multiple genera. In addition, we characterize the diversity of secretion systems and traits linked to host invasion encoded by the different species, finding evidence of a widespread horizontal gene transfer. While genus clusters were found to encode different metabolic capabilities, species more related to L. pneumophila were generically characterized by a more complete metabolism and a lower amount of auxotrophies, calling for the redesign of cultivation strategies to account for less studied taxa. Finally, a genome-informed analysis of the species environmental distribution revealed that, despite species with similar metabolic capabilities tending to co-occur in the same niches, most species have distinct environmental distributions. Together, our results shed light on the ecology of these microorganisms and highlight the diversity of traits which can occur in closely related facultative intracellular bacteria.