Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
Phagocytosis is a key process of the immune system. The human pathogen Klebsiella pneumoniae is a well known example of a pathogen highly resistant to phagocytosis. A wealth of evidence demonstrates that the capsule polysaccharide (CPS) plays a crucial role in resistance to phagocytosis. The amoeba...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2013-01-01
|
| Series: | PLoS ONE |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23457627/pdf/?tool=EBI |
| _version_ | 1818459811110453248 |
|---|---|
| author | Catalina March Victoria Cano David Moranta Enrique Llobet Camino Pérez-Gutiérrez Juan M Tomás Teresa Suárez Junkal Garmendia José A Bengoechea |
| author_facet | Catalina March Victoria Cano David Moranta Enrique Llobet Camino Pérez-Gutiérrez Juan M Tomás Teresa Suárez Junkal Garmendia José A Bengoechea |
| author_sort | Catalina March |
| collection | DOAJ |
| description | Phagocytosis is a key process of the immune system. The human pathogen Klebsiella pneumoniae is a well known example of a pathogen highly resistant to phagocytosis. A wealth of evidence demonstrates that the capsule polysaccharide (CPS) plays a crucial role in resistance to phagocytosis. The amoeba Dictyostelium discoideum shares with mammalian macrophages the ability to phagocytose and kill bacteria. The fact that K. pneumoniae is ubiquitous in nature and, therefore, should avoid predation by amoebae, poses the question whether K. pneumoniae employs similar means to counteract amoebae and mammalian phagocytes. Here we developed an assay to evaluate K. pneumoniae-D. discoideum interaction. The richness of the growth medium affected the threshold at which the cps mutant was permissive for Dictyostelium and only at lower nutrient concentrations the cps mutant was susceptible to predation by amoebae. Given the critical role of bacterial surface elements on host-pathogen interactions, we explored the possible contribution of the lipopolysaccharide (LPS) and outer membrane proteins (OMPs) to combat phagoyctosis by D. discoideum. We uncover that, in addition to the CPS, the LPS O-polysaccharide and the first core sugar participate in Klebsiella resistance to predation by D. discoideum. K. pneumoniae LPS lipid A decorations are also necessary to avoid predation by amoebae although PagP-dependent palmitoylation plays a more important role than the lipid A modification with aminoarabinose. Mutants lacking OMPs OmpA or OmpK36 were also permissive for D. discoideium growth. Except the LPS O-polysaccharide mutants, all mutants were more susceptible to phagocytosis by mouse alveolar macrophages. Finally, we found a correlation between virulence, using the pneumonia mouse model, and resistance to phagocytosis. Altogether, this work reveals novel K. pneumoniae determinants involved in resistance to phagocytosis and supports the notion that Dictyostelium amoebae might be useful as host model to measure K. pneumoniae virulence and not only phagocytosis. |
| first_indexed | 2024-12-14T23:20:17Z |
| format | Article |
| id | doaj.art-1a97845a55a84df99050fe0bfb981877 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-14T23:20:17Z |
| publishDate | 2013-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-1a97845a55a84df99050fe0bfb9818772022-12-21T22:43:59ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0182e5684710.1371/journal.pone.0056847Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.Catalina MarchVictoria CanoDavid MorantaEnrique LlobetCamino Pérez-GutiérrezJuan M TomásTeresa SuárezJunkal GarmendiaJosé A BengoecheaPhagocytosis is a key process of the immune system. The human pathogen Klebsiella pneumoniae is a well known example of a pathogen highly resistant to phagocytosis. A wealth of evidence demonstrates that the capsule polysaccharide (CPS) plays a crucial role in resistance to phagocytosis. The amoeba Dictyostelium discoideum shares with mammalian macrophages the ability to phagocytose and kill bacteria. The fact that K. pneumoniae is ubiquitous in nature and, therefore, should avoid predation by amoebae, poses the question whether K. pneumoniae employs similar means to counteract amoebae and mammalian phagocytes. Here we developed an assay to evaluate K. pneumoniae-D. discoideum interaction. The richness of the growth medium affected the threshold at which the cps mutant was permissive for Dictyostelium and only at lower nutrient concentrations the cps mutant was susceptible to predation by amoebae. Given the critical role of bacterial surface elements on host-pathogen interactions, we explored the possible contribution of the lipopolysaccharide (LPS) and outer membrane proteins (OMPs) to combat phagoyctosis by D. discoideum. We uncover that, in addition to the CPS, the LPS O-polysaccharide and the first core sugar participate in Klebsiella resistance to predation by D. discoideum. K. pneumoniae LPS lipid A decorations are also necessary to avoid predation by amoebae although PagP-dependent palmitoylation plays a more important role than the lipid A modification with aminoarabinose. Mutants lacking OMPs OmpA or OmpK36 were also permissive for D. discoideium growth. Except the LPS O-polysaccharide mutants, all mutants were more susceptible to phagocytosis by mouse alveolar macrophages. Finally, we found a correlation between virulence, using the pneumonia mouse model, and resistance to phagocytosis. Altogether, this work reveals novel K. pneumoniae determinants involved in resistance to phagocytosis and supports the notion that Dictyostelium amoebae might be useful as host model to measure K. pneumoniae virulence and not only phagocytosis.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23457627/pdf/?tool=EBI |
| spellingShingle | Catalina March Victoria Cano David Moranta Enrique Llobet Camino Pérez-Gutiérrez Juan M Tomás Teresa Suárez Junkal Garmendia José A Bengoechea Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. PLoS ONE |
| title | Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. |
| title_full | Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. |
| title_fullStr | Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. |
| title_full_unstemmed | Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. |
| title_short | Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. |
| title_sort | role of bacterial surface structures on the interaction of klebsiella pneumoniae with phagocytes |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23457627/pdf/?tool=EBI |
| work_keys_str_mv | AT catalinamarch roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT victoriacano roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT davidmoranta roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT enriquellobet roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT caminoperezgutierrez roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT juanmtomas roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT teresasuarez roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT junkalgarmendia roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes AT joseabengoechea roleofbacterialsurfacestructuresontheinteractionofklebsiellapneumoniaewithphagocytes |