The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces.
Since mucosal surfaces may be simultaneously colonized by multiple species, the success of an organism may be determined by its ability to compete with co-inhabitants of its niche. To explore the contribution of host factors to polymicrobial competition, a murine model was used to study the initiati...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2005-09-01
|
| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.0010001 |
| _version_ | 1797830928175726592 |
|---|---|
| author | Elena S Lysenko Adam J Ratner Aaron L Nelson Jeffrey N Weiser |
| author_facet | Elena S Lysenko Adam J Ratner Aaron L Nelson Jeffrey N Weiser |
| author_sort | Elena S Lysenko |
| collection | DOAJ |
| description | Since mucosal surfaces may be simultaneously colonized by multiple species, the success of an organism may be determined by its ability to compete with co-inhabitants of its niche. To explore the contribution of host factors to polymicrobial competition, a murine model was used to study the initiation of colonization by Haemophilus influenzae and Streptococcus pneumoniae. Both bacterial species, which occupy a similar microenvironment within the nasopharynx, persisted during colonization when given individually. Co-colonization, however, resulted in rapid clearance of S. pneumoniae from the upper respiratory tract, associated with increased recruitment of neutrophils into paranasal spaces. Systemic depletion of either neutrophil-like cells or complement was sufficient to eliminate this competitive effect, indicating that clearance was likely due to enhanced opsonophagocytic killing. The hypothesis that modulation of opsonophagocytic activity was responsible for host-mediated competition was tested using in vitro killing assays with elicited neutrophil-like cells. Components of H. influenzae (but not S. pneumoniae) stimulated complement-dependent phagocytic killing of S. pneumoniae. Thus, the recruitment and activation of neutrophils through selective microbial pattern recognition may underlie the H. influenzae-induced clearance of S. pneumoniae. This study demonstrates how innate immune responses may mediate competitive interactions between species and dictate the composition of the colonizing flora. |
| first_indexed | 2024-04-09T13:44:51Z |
| format | Article |
| id | doaj.art-99161056f5b24392a43038bb9689c6d6 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-04-09T13:44:51Z |
| publishDate | 2005-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-99161056f5b24392a43038bb9689c6d62023-05-09T05:32:07ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742005-09-0111e110.1371/journal.ppat.0010001The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces.Elena S LysenkoAdam J RatnerAaron L NelsonJeffrey N WeiserSince mucosal surfaces may be simultaneously colonized by multiple species, the success of an organism may be determined by its ability to compete with co-inhabitants of its niche. To explore the contribution of host factors to polymicrobial competition, a murine model was used to study the initiation of colonization by Haemophilus influenzae and Streptococcus pneumoniae. Both bacterial species, which occupy a similar microenvironment within the nasopharynx, persisted during colonization when given individually. Co-colonization, however, resulted in rapid clearance of S. pneumoniae from the upper respiratory tract, associated with increased recruitment of neutrophils into paranasal spaces. Systemic depletion of either neutrophil-like cells or complement was sufficient to eliminate this competitive effect, indicating that clearance was likely due to enhanced opsonophagocytic killing. The hypothesis that modulation of opsonophagocytic activity was responsible for host-mediated competition was tested using in vitro killing assays with elicited neutrophil-like cells. Components of H. influenzae (but not S. pneumoniae) stimulated complement-dependent phagocytic killing of S. pneumoniae. Thus, the recruitment and activation of neutrophils through selective microbial pattern recognition may underlie the H. influenzae-induced clearance of S. pneumoniae. This study demonstrates how innate immune responses may mediate competitive interactions between species and dictate the composition of the colonizing flora.https://doi.org/10.1371/journal.ppat.0010001 |
| spellingShingle | Elena S Lysenko Adam J Ratner Aaron L Nelson Jeffrey N Weiser The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PLoS Pathogens |
| title | The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. |
| title_full | The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. |
| title_fullStr | The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. |
| title_full_unstemmed | The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. |
| title_short | The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. |
| title_sort | role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces |
| url | https://doi.org/10.1371/journal.ppat.0010001 |
| work_keys_str_mv | AT elenaslysenko theroleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT adamjratner theroleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT aaronlnelson theroleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT jeffreynweiser theroleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT elenaslysenko roleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT adamjratner roleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT aaronlnelson roleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces AT jeffreynweiser roleofinnateimmuneresponsesintheoutcomeofinterspeciescompetitionforcolonizationofmucosalsurfaces |