We investigated whether nematodes contribute to the persistence, differentiation and amplification of Legionella species in soil, an emerging source for Legionnaires’ disease. Here we show that Legionella spp. colonize the intestinal tracts of Caenorhabditis nematodes leading to worm death. Susceptibility to Legionella is influenced by innate immune responses governed by the p38 mitogen-activated protein kinase and insulin/insulin growth factor-1 receptor signaling pathways. We also show that L. pneumophila colonizes the intestinal tract of nematodes cultivated in soil. To distinguish between transient infection and persistence, plate-fed and soil-extracted nematodes fed fluorescent strains of L. pneumophila were analyzed. Bacteria replicated within the nematode intestinal tract, did not invade surrounding tissue, and were excreted as differentiated forms that were transmitted to offspring. Interestingly, the ultrastructural features of the differentiated bacterial forms were similar to cyst-like forms observed within protozoa, amoeba and mammalian cell lines. While intestinal colonization of L. pneumophila dotA and icmT mutant strains did not alter the survival rate of nematodes in comparison to wild-type strains, nematodes colonized with the dot/icm mutant strains exhibited significantly increased levels of germline apoptosis. Taken together, these studies show that nematodes may serve as natural hosts for these organisms and thereby contribute to their dissemination in the environment and suggest that the remarkable ability of L. pneumophila to subvert host cell signaling and evade mammalian immune responses evolved through the natural selection associated with cycling between protozoan and metazoan hosts.

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