Heavy Ion Radiation Directly Induced the Shift of Oral Microbiota and Increased the Cariogenicity of <i>Streptococcus mutans</i>

作者全名："Wang, Zheng; Yang, Ge; Zhou, Xuedong; Peng, Xian; Li, Mingyun; Zhang, Miaomiao; Lu, Dong; Yang, Deqin; Cheng, Lei; Ren, Biao"

作者地址："[Wang, Zheng; Yang, Ge; Zhou, Xuedong; Peng, Xian; Li, Mingyun; Cheng, Lei; Ren, Biao] Sichuan Univ, State Key Lab Oral Dis, Chengdu, Peoples R China; [Wang, Zheng; Yang, Ge; Zhou, Xuedong; Peng, Xian; Li, Mingyun; Cheng, Lei; Ren, Biao] Sichuan Univ, Natl Clin Res Ctr Oral Dis, Chengdu, Peoples R China; [Wang, Zheng; Yang, Ge; Zhou, Xuedong; Peng, Xian; Li, Mingyun; Cheng, Lei; Ren, Biao] Sichuan Univ, West China Hosp Stomatol, Chengdu, Peoples R China; [Zhang, Miaomiao; Lu, Dong] Chinese Acad Sci, Inst Modern Phys, Lanzhou, Peoples R China; [Wang, Zheng; Yang, Deqin] Chongqing Med Univ, Coll Stomatol, Chongqing, Peoples R China"

通信作者："Cheng, L; Ren, B (通讯作者)，Sichuan Univ, State Key Lab Oral Dis, Chengdu, Peoples R China.; Cheng, L; Ren, B (通讯作者)，Sichuan Univ, Natl Clin Res Ctr Oral Dis, Chengdu, Peoples R China.; Cheng, L; Ren, B (通讯作者)，Sichuan Univ, West China Hosp Stomatol, Chengdu, Peoples R China."

来源：MICROBIOLOGY SPECTRUM

ESI学科分类：MICROBIOLOGY

WOS号：WOS:001005287300001

JCR分区：Q2

影响因子：3.7

年份：2023

卷号：11

期号：4

开始页：　

结束页：　

文献类型：Article

关键词：heavy ion; Streptococcus mutans; oral microbiota

摘要："The oral microbiome is crucial to understanding the pathogenesis of radiation caries. Although heavy ion radiation has been used to treat head and neck cancers in some proton therapy centers, its correlation with dental caries, especially its direct effects on the oral microbiome and cariogenic pathogens, has not been reported previously. Radiation caries is one of the most common complications of head and neck radiotherapy. A shift in the oral microbiota is the main factor of radiation caries. A new form of biosafe radiation, heavy ion radiation, is increasingly being applied in clinical treatment due to its superior depth-dose distribution and biological effects. However, how heavy ion radiation directly impacts the oral microbiota and the progress of radiation caries are unknown. Here, unstimulated saliva samples from both healthy and caries volunteers and caries-related bacteria were directly exposed to therapeutic doses of heavy ion radiation to determine the effects of radiation on oral microbiota composition and bacterial cariogenicity. Heavy ion radiation significantly decreased the richness and diversity of oral microbiota from both healthy and caries volunteers, and a higher percentage of Streptococcus was detected in radiation groups. In addition, heavy ion radiation significantly enhanced the cariogenicity of saliva-derived biofilms, including the ratios of the genus Streptococcus and biofilm formation. In the Streptococcus mutans-Streptococcus sanguinis dual-species biofilms, heavy ion radiation increased the ratio of S. mutans. Next, S. mutans was directly exposed to heavy ions, and the radiation significantly upregulated the gtfC and gtfD cariogenic virulence genes to enhance the biofilm formation and exopolysaccharides synthesis of S. mutans. Our study demonstrated, for the first time, that direct exposure to heavy ion radiation can disrupt the oral microbial diversity and balance of dual-species biofilms by increasing the virulence of S. mutans, increasing its cariogenicity, indicating a potential correlation between heavy ions and radiation caries.IMPORTANCE The oral microbiome is crucial to understanding the pathogenesis of radiation caries. Although heavy ion radiation has been used to treat head and neck cancers in some proton therapy centers, its correlation with dental caries, especially its direct effects on the oral microbiome and cariogenic pathogens, has not been reported previously. Here, we showed that the heavy ion radiation directly shifted the oral microbiota from a balanced state to a caries-associated state by increasing the cariogenic virulence of S. mutans. Our study highlighted the direct effect of heavy ion radiation on oral microbiota and the cariogenicity of oral microbes for the first time."

基金机构："National Natural Science Foundation of China [82071106, 81600858, 81991500, 81991501]; Key Research and Development Projects of the Science and Technology Department of Sichuan Province [2021YFQ0064]; Technology Innovation R&D Project of Chengdu [2022-YF05-01401-SN]; West China School/Hospital of Stomatology, Sichuan University [RD-03-202308]; Talent Program of the West China School of Stomatology [RCDWJS2021-19]"

基金资助正文："We thank our colleagues at HIRFL for providing the high-quality heavy ion beams. This study was supported by the National Natural Science Foundation of China grants (82071106 to L.C.; 81600858, 81991500, and 81991501 to B.R.), the Key Research and Development Projects of the Science and Technology Department of Sichuan Province (2021YFQ0064 to B.R.), the Technology Innovation R&D Project of Chengdu (2022-YF05-01401-SN to B.R.), research funding from the West China School/Hospital of Stomatology, Sichuan University (RD-03-202308 to L.C.), and the Talent Program of the West China School of Stomatology (RCDWJS2021-19 to L.C.). M.Z., D.L., B.R., and L.C. conceived and designed the research. Z.W. and G.Y. conducted experiments. X.Z., M.L. and X.P. analyzed the data. Z.W. wrote the manuscript. D.Y., B.R., and L.C. critically revised the manuscript. All authors read and approved the manuscript. We declare that we have no conflicts of interest."