Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro
Background Streptococcus oralis is a commensal bacterium and an early biofilm coloniser found in the human oral cavity. One of the biofilm matrix constituents is bacterial extracellular DNA (eDNA). Neutrophils are innate immune cells that respond to biofilms, employing antimicrobial mechanisms such...
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2025-12-01
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| Series: | Journal of Oral Microbiology |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/20002297.2025.2453986 |
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| author | Basmah M. Almaarik Rizwan Ali Paul R. Cooper Michael R. Milward Josefine Hirschfeld |
| author_facet | Basmah M. Almaarik Rizwan Ali Paul R. Cooper Michael R. Milward Josefine Hirschfeld |
| author_sort | Basmah M. Almaarik |
| collection | DOAJ |
| description | Background Streptococcus oralis is a commensal bacterium and an early biofilm coloniser found in the human oral cavity. One of the biofilm matrix constituents is bacterial extracellular DNA (eDNA). Neutrophils are innate immune cells that respond to biofilms, employing antimicrobial mechanisms such as neutrophil extracellular trap (NET) and reactive oxygen species (ROS) release. Here, bidirectional effects of neutrophils on S. oralis biofilms were investigated.Materials and methods Isolated neutrophils were introduced to S. oralis biofilms at different stages of biofilm development. Biofilm quantity was assessed by crystal violet technique, confocal microscopy and CFU enumeration. Surface adhesion during shear stress was quantified by spectrophotometry. Bacterial and neutrophil extracellular DNA within biofilms and ROS production were analysed using fluorescence and luminescence assays, and neutrophil-eDNA interactions were investigated by flow cytometry and fluorescence microscopy.Results Neutrophils decreased S. oralis biofilm quantity transiently and reduced eDNA but did not affect biofilm surface adhesion. Unexpectedly, CFUs were increased by neutrophils. Bacterial DNA was found to co-localise with neutrophil membranes. Neutrophils produced elevated total and intracellular ROS, however, no NETs in response to biofilms.Conclusion Neutrophils in vitro are not excessively activated by S. oralis biofilms but are able to reduce biofilm quantity in the short-term, possibly through interfering with eDNA. |
| format | Article |
| id | doaj-art-efeb666daf7041b19bf8c08b27a68d69 |
| institution | Kabale University |
| issn | 2000-2297 |
| language | English |
| publishDate | 2025-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Journal of Oral Microbiology |
| spelling | doaj-art-efeb666daf7041b19bf8c08b27a68d692025-01-23T17:32:16ZengTaylor & Francis GroupJournal of Oral Microbiology2000-22972025-12-0117110.1080/20002297.2025.2453986Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitroBasmah M. Almaarik0Rizwan Ali1Paul R. Cooper2Michael R. Milward3Josefine Hirschfeld4Clinical Laboratory Science Department (CLS), College of Applied Medical Sciences (CAMS), King Saud University (KSU), Riyadh, Saudi ArabiaMedical Research Core Facility and Platforms, King Abdullah International Medical Research Center (KAIMRC), King Saud Bin Abdulaziz University for Health Sciences (KSAU-HS), Riyadh, Saudi ArabiaDepartment of Oral Sciences, Sir John Walsh Research Institute, Faculty of Dentistry, University of Otago, Dunedin, New ZealandPeriodontal Research Group, Department of Dentistry, School of Health Sciences, College of Medicine and Health, University of Birmingham, Edgbaston, UKPeriodontal Research Group, Department of Dentistry, School of Health Sciences, College of Medicine and Health, University of Birmingham, Edgbaston, UKBackground Streptococcus oralis is a commensal bacterium and an early biofilm coloniser found in the human oral cavity. One of the biofilm matrix constituents is bacterial extracellular DNA (eDNA). Neutrophils are innate immune cells that respond to biofilms, employing antimicrobial mechanisms such as neutrophil extracellular trap (NET) and reactive oxygen species (ROS) release. Here, bidirectional effects of neutrophils on S. oralis biofilms were investigated.Materials and methods Isolated neutrophils were introduced to S. oralis biofilms at different stages of biofilm development. Biofilm quantity was assessed by crystal violet technique, confocal microscopy and CFU enumeration. Surface adhesion during shear stress was quantified by spectrophotometry. Bacterial and neutrophil extracellular DNA within biofilms and ROS production were analysed using fluorescence and luminescence assays, and neutrophil-eDNA interactions were investigated by flow cytometry and fluorescence microscopy.Results Neutrophils decreased S. oralis biofilm quantity transiently and reduced eDNA but did not affect biofilm surface adhesion. Unexpectedly, CFUs were increased by neutrophils. Bacterial DNA was found to co-localise with neutrophil membranes. Neutrophils produced elevated total and intracellular ROS, however, no NETs in response to biofilms.Conclusion Neutrophils in vitro are not excessively activated by S. oralis biofilms but are able to reduce biofilm quantity in the short-term, possibly through interfering with eDNA.https://www.tandfonline.com/doi/10.1080/20002297.2025.2453986Streptococcus oralisbiofilmneutrophilseDNAperiodontitis |
| spellingShingle | Basmah M. Almaarik Rizwan Ali Paul R. Cooper Michael R. Milward Josefine Hirschfeld Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro Journal of Oral Microbiology Streptococcus oralis biofilm neutrophils eDNA periodontitis |
| title | Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro |
| title_full | Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro |
| title_fullStr | Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro |
| title_full_unstemmed | Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro |
| title_short | Bidirectional effects of neutrophils on Streptococcus oralis biofilms in vitro |
| title_sort | bidirectional effects of neutrophils on streptococcus oralis biofilms in vitro |
| topic | Streptococcus oralis biofilm neutrophils eDNA periodontitis |
| url | https://www.tandfonline.com/doi/10.1080/20002297.2025.2453986 |
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