Dongyeop Kim, Tatsuro Ito, Anderson Hara, Yong Li, Jens Kreth, Hyun Koo
{"title":"产生高 H2 O2 的共生链球菌的拮抗相互作用可调节变异链球菌的龋齿发展。","authors":"Dongyeop Kim, Tatsuro Ito, Anderson Hara, Yong Li, Jens Kreth, Hyun Koo","doi":"10.1111/omi.12394","DOIUrl":null,"url":null,"abstract":"<p><p>Dental caries (tooth-decay) is caused by biofilms harboring polymicrobial communities on teeth that leads to the onset of localized areas of enamel demineralization. Streptococcus mutans has been clinically associated with severe caries in childhood. Although commensal bacteria can combat S. mutans using self-generated antimicrobials such as hydrogen peroxide (H<sub>2</sub> O<sub>2</sub> ), constant sugar-rich diet consumption disrupts microbial homeostasis shifting toward cariogenic community. Recently, Streptococcus oralis subsp. tigurinus strain J22, an oral isolate, was identified as a uniquely potent H<sub>2</sub> O<sub>2</sub> producer. Here, we assess whether a high H<sub>2</sub> O<sub>2</sub> -producing commensal streptococcus can modulate the spatial organization and virulence of S. mutans within biofilms. Using an experimental biofilm model, we find that the presence of S. oralis J22 can effectively inhibit the clustering, accumulation, and spatial organization of S. mutans on ex vivo human tooth surface, resulting in significant reduction of enamel demineralization. Notably, the generation of H<sub>2</sub> O<sub>2</sub> via pyruvate oxidase (SpxB) from S. oralis J22 is not repressed by sugars (a common repressor in other mitis group streptococci), resulting in enhanced inhibition of S. mutans growth (vs. Streptococcus gordonii). We further investigate its impact on biofilm virulence using an in vivo rodent caries model under sugar-rich diet. Coinfection of S. mutans with S. oralis results in reduced caries development compared to either species infected alone, whereas coinfection with S. gordonii has negligible effects, suggesting that the presence of an efficient, high H<sub>2</sub> O<sub>2</sub> -producer can disrupt S. mutans virulence. This work demonstrates that oral isolates with unusual high H<sub>2</sub> O<sub>2</sub> production may be capable of modulating biofilm cariogenicity in vivo. The findings also highlight the importance of bacterial antagonistic interactions within polymicrobial communities in health and in disease-causing state.</p>","PeriodicalId":2,"journal":{"name":"ACS Applied Bio Materials","volume":" ","pages":"244-255"},"PeriodicalIF":4.6000,"publicationDate":"2022-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Antagonistic interactions by a high H<sub>2</sub> O<sub>2</sub> -producing commensal streptococcus modulate caries development by Streptococcus mutans.\",\"authors\":\"Dongyeop Kim, Tatsuro Ito, Anderson Hara, Yong Li, Jens Kreth, Hyun Koo\",\"doi\":\"10.1111/omi.12394\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Dental caries (tooth-decay) is caused by biofilms harboring polymicrobial communities on teeth that leads to the onset of localized areas of enamel demineralization. Streptococcus mutans has been clinically associated with severe caries in childhood. Although commensal bacteria can combat S. mutans using self-generated antimicrobials such as hydrogen peroxide (H<sub>2</sub> O<sub>2</sub> ), constant sugar-rich diet consumption disrupts microbial homeostasis shifting toward cariogenic community. Recently, Streptococcus oralis subsp. tigurinus strain J22, an oral isolate, was identified as a uniquely potent H<sub>2</sub> O<sub>2</sub> producer. Here, we assess whether a high H<sub>2</sub> O<sub>2</sub> -producing commensal streptococcus can modulate the spatial organization and virulence of S. mutans within biofilms. Using an experimental biofilm model, we find that the presence of S. oralis J22 can effectively inhibit the clustering, accumulation, and spatial organization of S. mutans on ex vivo human tooth surface, resulting in significant reduction of enamel demineralization. Notably, the generation of H<sub>2</sub> O<sub>2</sub> via pyruvate oxidase (SpxB) from S. oralis J22 is not repressed by sugars (a common repressor in other mitis group streptococci), resulting in enhanced inhibition of S. mutans growth (vs. Streptococcus gordonii). We further investigate its impact on biofilm virulence using an in vivo rodent caries model under sugar-rich diet. Coinfection of S. mutans with S. oralis results in reduced caries development compared to either species infected alone, whereas coinfection with S. gordonii has negligible effects, suggesting that the presence of an efficient, high H<sub>2</sub> O<sub>2</sub> -producer can disrupt S. mutans virulence. This work demonstrates that oral isolates with unusual high H<sub>2</sub> O<sub>2</sub> production may be capable of modulating biofilm cariogenicity in vivo. The findings also highlight the importance of bacterial antagonistic interactions within polymicrobial communities in health and in disease-causing state.</p>\",\"PeriodicalId\":2,\"journal\":{\"name\":\"ACS Applied Bio Materials\",\"volume\":\" \",\"pages\":\"244-255\"},\"PeriodicalIF\":4.6000,\"publicationDate\":\"2022-12-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"ACS Applied Bio Materials\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1111/omi.12394\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2022/10/11 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q2\",\"JCRName\":\"MATERIALS SCIENCE, BIOMATERIALS\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"ACS Applied Bio Materials","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1111/omi.12394","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2022/10/11 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"MATERIALS SCIENCE, BIOMATERIALS","Score":null,"Total":0}
Antagonistic interactions by a high H2 O2 -producing commensal streptococcus modulate caries development by Streptococcus mutans.
Dental caries (tooth-decay) is caused by biofilms harboring polymicrobial communities on teeth that leads to the onset of localized areas of enamel demineralization. Streptococcus mutans has been clinically associated with severe caries in childhood. Although commensal bacteria can combat S. mutans using self-generated antimicrobials such as hydrogen peroxide (H2 O2 ), constant sugar-rich diet consumption disrupts microbial homeostasis shifting toward cariogenic community. Recently, Streptococcus oralis subsp. tigurinus strain J22, an oral isolate, was identified as a uniquely potent H2 O2 producer. Here, we assess whether a high H2 O2 -producing commensal streptococcus can modulate the spatial organization and virulence of S. mutans within biofilms. Using an experimental biofilm model, we find that the presence of S. oralis J22 can effectively inhibit the clustering, accumulation, and spatial organization of S. mutans on ex vivo human tooth surface, resulting in significant reduction of enamel demineralization. Notably, the generation of H2 O2 via pyruvate oxidase (SpxB) from S. oralis J22 is not repressed by sugars (a common repressor in other mitis group streptococci), resulting in enhanced inhibition of S. mutans growth (vs. Streptococcus gordonii). We further investigate its impact on biofilm virulence using an in vivo rodent caries model under sugar-rich diet. Coinfection of S. mutans with S. oralis results in reduced caries development compared to either species infected alone, whereas coinfection with S. gordonii has negligible effects, suggesting that the presence of an efficient, high H2 O2 -producer can disrupt S. mutans virulence. This work demonstrates that oral isolates with unusual high H2 O2 production may be capable of modulating biofilm cariogenicity in vivo. The findings also highlight the importance of bacterial antagonistic interactions within polymicrobial communities in health and in disease-causing state.
期刊介绍:
ACS Applied Bio Materials is an interdisciplinary journal publishing original research covering all aspects of biomaterials and biointerfaces including and beyond the traditional biosensing, biomedical and therapeutic applications.
The journal is devoted to reports of new and original experimental and theoretical research of an applied nature that integrates knowledge in the areas of materials, engineering, physics, bioscience, and chemistry into important bio applications. The journal is specifically interested in work that addresses the relationship between structure and function and assesses the stability and degradation of materials under relevant environmental and biological conditions.