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Genomics can provide the basis for understanding the evolution of emerging, lethal human pathogens such as  Legionella pneumophila , the causative agent of Legionnaires’ disease. This bacterium replicates within amoebae and persists in the environment as a free-living microbe. Among the many  Legionella  species described,  L. pneumophila  is associated with 90% of human disease and within the 15 serogroups (Sg),  L. pneumophila  Sg1 causes over 84% of Legionnaires’ disease worldwide. Why  L. pneumophila  Sg1 is so predominant is unknown. Here, we report the first comprehensive screen of the gene content of 217  L. pneumophila  and 32 non- L. pneumophila  strains isolated from humans and the environment using a  Legionella  DNA-array. Strikingly, we uncovered a high conservation of virulence- and eukaryotic-like genes, indicating strong environmental selection pressures for their preservation. No specific hybridization profile differentiated clinical and environmental strains or strains of different serogroups. Surprisingly, the gene cluster coding the determinants of the core and the O side-chain synthesis of the lipopolysaccaride (LPS cluster) determining Sg1 was present in diverse genomic backgrounds, strongly implicating the LPS of Sg1 itself as a principal cause of the high prevalence of Sg1 strains in human disease and suggesting that the LPS cluster can be transferred horizontally. Genomic analysis also revealed that  L. pneumophila  is a genetically diverse species, in part due to horizontal gene transfer of mobile genetic elements among  L. pneumophila  strains, but also between different  Legionella  species. However, the genomic background also plays a role in disease causation as demonstrated by the identification of a globally distributed epidemic strain exhibiting the genotype of the sequenced  L. pneumophila  strain Paris.

Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species