Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study
ObjectiveThis study aimed to establish an in vitro model simulating periodontal biofilm architecture with three representative periodontal pathogens and evaluate its systemic impact through oral gavage administration in C57BL/6 mice. The findings provide mechanistic insights into the oral-gut axis d...
Saved in:
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2025-08-01
|
| Series: | Frontiers in Cellular and Infection Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2025.1589055/full |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850043831229087744 |
|---|---|
| author | Lan Huang Song Ge Kun Yang Lian Duan Li Gao Yu Zhen Li Yu Shi Yi |
| author_facet | Lan Huang Song Ge Kun Yang Lian Duan Li Gao Yu Zhen Li Yu Shi Yi |
| author_sort | Lan Huang |
| collection | DOAJ |
| description | ObjectiveThis study aimed to establish an in vitro model simulating periodontal biofilm architecture with three representative periodontal pathogens and evaluate its systemic impact through oral gavage administration in C57BL/6 mice. The findings provide mechanistic insights into the oral-gut axis dysbiosis, elucidating potential pathways linking periodontal inflammation to gastrointestinal pathophysiology.MethodsFifty 7-week-old male C57BL/6 mice were randomized into five groups(n=10/group): control (H), F. nucleatum (F), P.gingivalis (P), S.sanguinis (S) and biofilm (BF, F.n + P.g + S.s) groups. Mice were gavaged twice weekly for 6 weeks with 1×109 CFU (F, P, BF groups) and 1×108 CFU (S group) of bacterial suspensions or PBS (H group). Post-intervention, fecal and colon tissues were collected for 16S rRNA sequencing, H&E staining, immunohistochemistry (Occludin expression), and qRT-PCR analysis of inflammatory markers(IL18, TNF-α, IL-1β, B220, F4/80, NOS2, ARG1).ResultsA stable in vitro three-species biofilm model was successfully established to mimic the ecology of periodontal plaque. Gavage with F.n, P.g or the biofilm consortium (BF group) induced intestinal barrier disruption and elevated pro-inflammatory cytokines levels. PCR indicated a significant increase in the expression of IL-1β, TNF-α, B220, F4/80, and NOS2 in the P group (P < 0.001), while Arg-1 expression exhibited a significant decrease (P < 0.01). In the BF group, only TNF-α expression demonstrated a significant increase (P < 0.01). The expression of occludin is significantly reduced in the F/P/BF group, with the most pronounced decrease observed in the P group (P < 0.01). Gut microbiota alterations occurred in all groups. At the phylum level, the Firmicutes/Bacteroidetes (F/B) ratio increased in all three groups (F/P/BF group). Proteobacteria abundance rose substantially in the P group, while Desulfovibrio increased and Verrucomicrobia decreased in the F/P/BF and F/S groups, respectively. Genus-level analysis showed reduced Muribaculaceae in the F/P/BF group, alongside elevated pro-inflammatory bacteria (e.g., Enterococcus, Acinetobacter) and diminished beneficial bacteria (e.g., Bifidobacterium, Parabacteroides).ConclusionThese findings demonstrate that periodontal pathogens induce gut barrier compromise through microbiome-driven immunomodulation, with P. gingivalis exhibiting predominant pro-inflammatory effects. |
| format | Article |
| id | doaj-art-776bbd0a2d5c4df7a280f8b32a6c0762 |
| institution | DOAJ |
| issn | 2235-2988 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj-art-776bbd0a2d5c4df7a280f8b32a6c07622025-08-20T02:55:07ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882025-08-011510.3389/fcimb.2025.15890551589055Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic studyLan HuangSong GeKun YangLian DuanLi GaoYu Zhen LiYu Shi YiObjectiveThis study aimed to establish an in vitro model simulating periodontal biofilm architecture with three representative periodontal pathogens and evaluate its systemic impact through oral gavage administration in C57BL/6 mice. The findings provide mechanistic insights into the oral-gut axis dysbiosis, elucidating potential pathways linking periodontal inflammation to gastrointestinal pathophysiology.MethodsFifty 7-week-old male C57BL/6 mice were randomized into five groups(n=10/group): control (H), F. nucleatum (F), P.gingivalis (P), S.sanguinis (S) and biofilm (BF, F.n + P.g + S.s) groups. Mice were gavaged twice weekly for 6 weeks with 1×109 CFU (F, P, BF groups) and 1×108 CFU (S group) of bacterial suspensions or PBS (H group). Post-intervention, fecal and colon tissues were collected for 16S rRNA sequencing, H&E staining, immunohistochemistry (Occludin expression), and qRT-PCR analysis of inflammatory markers(IL18, TNF-α, IL-1β, B220, F4/80, NOS2, ARG1).ResultsA stable in vitro three-species biofilm model was successfully established to mimic the ecology of periodontal plaque. Gavage with F.n, P.g or the biofilm consortium (BF group) induced intestinal barrier disruption and elevated pro-inflammatory cytokines levels. PCR indicated a significant increase in the expression of IL-1β, TNF-α, B220, F4/80, and NOS2 in the P group (P < 0.001), while Arg-1 expression exhibited a significant decrease (P < 0.01). In the BF group, only TNF-α expression demonstrated a significant increase (P < 0.01). The expression of occludin is significantly reduced in the F/P/BF group, with the most pronounced decrease observed in the P group (P < 0.01). Gut microbiota alterations occurred in all groups. At the phylum level, the Firmicutes/Bacteroidetes (F/B) ratio increased in all three groups (F/P/BF group). Proteobacteria abundance rose substantially in the P group, while Desulfovibrio increased and Verrucomicrobia decreased in the F/P/BF and F/S groups, respectively. Genus-level analysis showed reduced Muribaculaceae in the F/P/BF group, alongside elevated pro-inflammatory bacteria (e.g., Enterococcus, Acinetobacter) and diminished beneficial bacteria (e.g., Bifidobacterium, Parabacteroides).ConclusionThese findings demonstrate that periodontal pathogens induce gut barrier compromise through microbiome-driven immunomodulation, with P. gingivalis exhibiting predominant pro-inflammatory effects.https://www.frontiersin.org/articles/10.3389/fcimb.2025.1589055/fullFusobacterium nucleatumPorphyromonas gingivalisStreptococcus sanguinisoral-gut axisdysbiosistight junctions |
| spellingShingle | Lan Huang Song Ge Kun Yang Lian Duan Li Gao Yu Zhen Li Yu Shi Yi Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study Frontiers in Cellular and Infection Microbiology Fusobacterium nucleatum Porphyromonas gingivalis Streptococcus sanguinis oral-gut axis dysbiosis tight junctions |
| title | Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study |
| title_full | Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study |
| title_fullStr | Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study |
| title_full_unstemmed | Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study |
| title_short | Effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice: a mechanistic study |
| title_sort | effects of oral gavage with periodontal pathogens and plaque biofilm on gut microbiota ecology and intestinal tissue architecture in mice a mechanistic study |
| topic | Fusobacterium nucleatum Porphyromonas gingivalis Streptococcus sanguinis oral-gut axis dysbiosis tight junctions |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2025.1589055/full |
| work_keys_str_mv | AT lanhuang effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy AT songge effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy AT kunyang effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy AT lianduan effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy AT ligao effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy AT yuzhenli effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy AT yushiyi effectsoforalgavagewithperiodontalpathogensandplaquebiofilmongutmicrobiotaecologyandintestinaltissuearchitectureinmiceamechanisticstudy |