| Summary: | Free-living nematodes harbor and disseminate various soil-borne bacterial pathogens. Whether they function as vectors or environmental reservoirs for the aquatic <i>L. pneumophila</i>, the causative agent of Legionnaires’ disease, is unknown. A survey screening of biofilms of natural (swimming lakes) and technical (cooling towers) water habitats in Germany revealed that nematodes can act as potential reservoirs, vectors or grazers of <i>L. pneumophila</i> in cooling towers. Consequently, the nematode species <i>Plectus similis</i> and <i>L. pneumophila</i> were isolated from the same cooling tower biofilm and taken into a monoxenic culture. Using pharyngeal pumping assays, potential feeding relationships between <i>P. similis</i> and different <i>L. pneumophila</i> strains and mutants were examined and compared with <i>Plectus</i> sp., a species isolated from a <i>L. pneumophila</i>-positive thermal source biofilm. The assays showed that bacterial suspensions and supernatants of the <i>L. pneumophila</i> cooling tower isolate KV02 decreased pumping rate and feeding activity in nematodes. However, assays investigating the hypothesized negative impact of <i>Legionella</i>’s major secretory protein ProA on pumping rate revealed opposite effects on nematodes, which points to a species-specific response to ProA. To extend the food chain by a further trophic level, <i>Acanthamoebae castellanii</i> infected with <i>L. pneumphila</i> KV02 were offered to nematodes. The pumping rates of <i>P. similis</i> increased when fed with <i>L. pneumophila</i>-infected <i>A. castellanii</i>, while <i>Plectus</i> sp. pumping rates were similar when fed either infected or non-infected <i>A. castellanii.</i> This study revealed that cooling towers are the main water bodies where <i>L. pneumophila</i> and free-living nematodes coexist and is the first step in elucidating the trophic links between coexisting taxa from that habitat. Investigating the <i>Legionella</i>–nematode–amoebae interactions underlined the importance of amoebae as reservoirs and transmission vehicles of the pathogen for nematode predators.
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