<i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link
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 (sw...
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| Format: | Article |
| Language: | English |
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MDPI AG
2023-03-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/11/3/738 |
| _version_ | 1797436198130548736 |
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| author | Christin Hemmerling Aurélie Labrosse Liliane Ruess Michael Steinert |
| author_facet | Christin Hemmerling Aurélie Labrosse Liliane Ruess Michael Steinert |
| author_sort | Christin Hemmerling |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-09T10:59:10Z |
| format | Article |
| id | doaj.art-602c988652e147d38a2f32555bd28bdc |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T10:59:10Z |
| publishDate | 2023-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-602c988652e147d38a2f32555bd28bdc2023-12-01T01:24:13ZengMDPI AGMicroorganisms2076-26072023-03-0111373810.3390/microorganisms11030738<i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic LinkChristin Hemmerling0Aurélie Labrosse1Liliane Ruess2Michael Steinert3Institute of Biology, Ecology, Humboldt Universität zu Berlin, Philippstraße 13, 10115 Berlin, GermanyInstitute of Microbiology, Technische Universität Braunschweig, Spielmannstraße 7, 38106 Braunschweig, GermanyInstitute of Biology, Ecology, Humboldt Universität zu Berlin, Philippstraße 13, 10115 Berlin, GermanyInstitute of Microbiology, Technische Universität Braunschweig, Spielmannstraße 7, 38106 Braunschweig, GermanyFree-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.https://www.mdpi.com/2076-2607/11/3/738<i>Legionella pneumophila</i>free-living nematodes<i>Plectus similis</i><i>Plectus</i> sp.<i>Acanthamoebae castellanii</i>pharyngeal pumping |
| spellingShingle | Christin Hemmerling Aurélie Labrosse Liliane Ruess Michael Steinert <i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link Microorganisms <i>Legionella pneumophila</i> free-living nematodes <i>Plectus similis</i> <i>Plectus</i> sp. <i>Acanthamoebae castellanii</i> pharyngeal pumping |
| title | <i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link |
| title_full | <i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link |
| title_fullStr | <i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link |
| title_full_unstemmed | <i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link |
| title_short | <i>Legionella pneumophila</i> and Free-Living Nematodes: Environmental Co-Occurrence and Trophic Link |
| title_sort | i legionella pneumophila i and free living nematodes environmental co occurrence and trophic link |
| topic | <i>Legionella pneumophila</i> free-living nematodes <i>Plectus similis</i> <i>Plectus</i> sp. <i>Acanthamoebae castellanii</i> pharyngeal pumping |
| url | https://www.mdpi.com/2076-2607/11/3/738 |
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