{"title":"在成人重度龋齿中,副龈上维龙菌是一种致病菌,可促进生物膜的毒力和变异链球菌的致龋性。","authors":"Yuan Wei, Yu Zhang, Yuan Zhuang, Yifei Tang, Hua Nie, Yequan Haung, Ting Liu, Weidong Yang, Fuhua Yan, Yanan Zhu","doi":"10.1128/spectrum.04318-23","DOIUrl":null,"url":null,"abstract":"<p><p>Adult severe caries (ASC) brings severe oral dysfunction and treatment difficulties to patients, and yet no clear pathogenic mechanism for it has been found. This study is focused on the composition of dental plaque microbiome profiles in order to identify disease-relevant species and to investigate into their interactions with the <i>S. mutans</i>. Samples of dental plaque were collected for metagenomic analysis. The acidification, aciduricity, oxidative stress tolerance, and <i>gtf</i> (glucosyltransferase) gene expression of <i>S. mutans</i> cocultured with <i>V. parvula</i> which was identified as ASC-related dominant bacterium. The biofilm formation and extracellular exopolysaccharide (EPS) synthesis of dual-strain were analyzed with scanning electron microscopy (SEM), crystal violet (CV) staining, live/dead bacterial staining, and confocal laser scanning microscopy (CLSM). Furthermore, rodent model experiments were performed to validate the <i>in vivo</i> cariogenicity of the dual-species biofilm. The most significantly abundant taxon found associated with ASC was <i>V. parvula</i>. <i>In vitro</i> experiments found that <i>V. parvula</i> can effectively promote <i>S. mutans</i> mature biofilm formation with enhanced acid resistance, hydrogen peroxide detoxicity, and biofilm virulence. Rodent model experiments revealed that <i>V. parvula</i> was incapable of causing disease on its own, but it significantly heightened the biofilm virulence of <i>S. mutans</i> when being co-infected and augmented the progression, quantity, and severity of dental caries. Our findings demonstrated that <i>V. parvula</i> may act as a synergistic pathobiont to modulate the metabolic activity, spatial structure, and pathogenicity of biofilms of <i>S. mutans</i> in the context of ASC.IMPORTANCEAdult severe caries (ASC), as a special type of acute caries, is rarely reported and its worthiness of further study is still in dispute. Yet studies on the etiology of severe caries in adults have not found a clear pathogenic mechanism for it. Knowledge of the oral microbiota is important for the treatment of dental caries. We discovered that the interaction between <i>V. parvula</i> and <i>S. mutans</i> augments the severity of dental caries <i>in vivo</i>, suggesting <i>V. parvula</i> may act as a synergistic pathobiont exacerbating biofilm virulence of <i>S. mutans</i> in ASC. Our findings may improve the understanding of ASC pathogenesis and are likely to provide a basis for planning appropriate therapeutic strategies.</p>","PeriodicalId":18670,"journal":{"name":"Microbiology spectrum","volume":null,"pages":null},"PeriodicalIF":3.7000,"publicationDate":"2024-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537095/pdf/","citationCount":"0","resultStr":"{\"title\":\"<i>Veillonella parvula</i> acts as a pathobiont promoting the biofilm virulence and cariogenicity of <i>Streptococcus mutans</i> in adult severe caries.\",\"authors\":\"Yuan Wei, Yu Zhang, Yuan Zhuang, Yifei Tang, Hua Nie, Yequan Haung, Ting Liu, Weidong Yang, Fuhua Yan, Yanan Zhu\",\"doi\":\"10.1128/spectrum.04318-23\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Adult severe caries (ASC) brings severe oral dysfunction and treatment difficulties to patients, and yet no clear pathogenic mechanism for it has been found. This study is focused on the composition of dental plaque microbiome profiles in order to identify disease-relevant species and to investigate into their interactions with the <i>S. mutans</i>. Samples of dental plaque were collected for metagenomic analysis. The acidification, aciduricity, oxidative stress tolerance, and <i>gtf</i> (glucosyltransferase) gene expression of <i>S. mutans</i> cocultured with <i>V. parvula</i> which was identified as ASC-related dominant bacterium. The biofilm formation and extracellular exopolysaccharide (EPS) synthesis of dual-strain were analyzed with scanning electron microscopy (SEM), crystal violet (CV) staining, live/dead bacterial staining, and confocal laser scanning microscopy (CLSM). Furthermore, rodent model experiments were performed to validate the <i>in vivo</i> cariogenicity of the dual-species biofilm. The most significantly abundant taxon found associated with ASC was <i>V. parvula</i>. <i>In vitro</i> experiments found that <i>V. parvula</i> can effectively promote <i>S. mutans</i> mature biofilm formation with enhanced acid resistance, hydrogen peroxide detoxicity, and biofilm virulence. Rodent model experiments revealed that <i>V. parvula</i> was incapable of causing disease on its own, but it significantly heightened the biofilm virulence of <i>S. mutans</i> when being co-infected and augmented the progression, quantity, and severity of dental caries. Our findings demonstrated that <i>V. parvula</i> may act as a synergistic pathobiont to modulate the metabolic activity, spatial structure, and pathogenicity of biofilms of <i>S. mutans</i> in the context of ASC.IMPORTANCEAdult severe caries (ASC), as a special type of acute caries, is rarely reported and its worthiness of further study is still in dispute. Yet studies on the etiology of severe caries in adults have not found a clear pathogenic mechanism for it. Knowledge of the oral microbiota is important for the treatment of dental caries. We discovered that the interaction between <i>V. parvula</i> and <i>S. mutans</i> augments the severity of dental caries <i>in vivo</i>, suggesting <i>V. parvula</i> may act as a synergistic pathobiont exacerbating biofilm virulence of <i>S. mutans</i> in ASC. Our findings may improve the understanding of ASC pathogenesis and are likely to provide a basis for planning appropriate therapeutic strategies.</p>\",\"PeriodicalId\":18670,\"journal\":{\"name\":\"Microbiology spectrum\",\"volume\":null,\"pages\":null},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2024-11-05\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537095/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Microbiology spectrum\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1128/spectrum.04318-23\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/9/30 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q2\",\"JCRName\":\"MICROBIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Microbiology spectrum","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/spectrum.04318-23","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/9/30 0:00:00","PubModel":"Epub","JCR":"Q2","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
成人严重龋齿(ASC)给患者带来了严重的口腔功能障碍和治疗困难,但至今尚未找到明确的致病机制。本研究的重点是牙菌斑微生物组的组成情况,以确定与疾病相关的物种,并研究它们与变异单胞菌的相互作用。研究人员采集了牙菌斑样本进行元基因组分析。与副噬菌体(V. parvula)共培养的变异棒状杆菌的酸化、酸度、氧化应激耐受性和葡萄糖基转移酶(gtf)基因表达情况,副噬菌体被确定为与 ASC 相关的优势菌。利用扫描电子显微镜(SEM)、水晶紫(CV)染色、活/死细菌染色和激光共聚焦扫描显微镜(CLSM)分析了双菌株的生物膜形成和细胞外多糖(EPS)合成。此外,还进行了啮齿动物模型试验,以验证双物种生物膜的体内致龋性。结果发现,与 ASC 相关的最多的类群是 V. parvula。体外实验发现,V. parvula 能有效促进 S. mutans 成熟生物膜的形成,并具有更强的耐酸性、过氧化氢解毒性和生物膜毒力。啮齿动物模型实验表明,副噬菌体本身不能致病,但当与变异棒状杆菌共同感染时,它能显著增强变异棒状杆菌的生物膜毒力,并能增加龋齿的发展、数量和严重程度。重要意义成人严重龋(ASC)作为急性龋病的一种特殊类型,鲜有报道,其是否值得进一步研究仍存在争议。然而,关于成人重度龋病因的研究尚未发现明确的致病机制。了解口腔微生物群对治疗龋齿非常重要。我们发现,V. parvula 和 S. mutans 之间的相互作用会增加体内龋齿的严重程度,这表明 V. parvula 可能是一种协同致病菌,会加剧 ASC 中 S. mutans 的生物膜毒力。我们的发现可能会加深对 ASC 发病机制的了解,并为制定适当的治疗策略提供依据。
Veillonella parvula acts as a pathobiont promoting the biofilm virulence and cariogenicity of Streptococcus mutans in adult severe caries.
Adult severe caries (ASC) brings severe oral dysfunction and treatment difficulties to patients, and yet no clear pathogenic mechanism for it has been found. This study is focused on the composition of dental plaque microbiome profiles in order to identify disease-relevant species and to investigate into their interactions with the S. mutans. Samples of dental plaque were collected for metagenomic analysis. The acidification, aciduricity, oxidative stress tolerance, and gtf (glucosyltransferase) gene expression of S. mutans cocultured with V. parvula which was identified as ASC-related dominant bacterium. The biofilm formation and extracellular exopolysaccharide (EPS) synthesis of dual-strain were analyzed with scanning electron microscopy (SEM), crystal violet (CV) staining, live/dead bacterial staining, and confocal laser scanning microscopy (CLSM). Furthermore, rodent model experiments were performed to validate the in vivo cariogenicity of the dual-species biofilm. The most significantly abundant taxon found associated with ASC was V. parvula. In vitro experiments found that V. parvula can effectively promote S. mutans mature biofilm formation with enhanced acid resistance, hydrogen peroxide detoxicity, and biofilm virulence. Rodent model experiments revealed that V. parvula was incapable of causing disease on its own, but it significantly heightened the biofilm virulence of S. mutans when being co-infected and augmented the progression, quantity, and severity of dental caries. Our findings demonstrated that V. parvula may act as a synergistic pathobiont to modulate the metabolic activity, spatial structure, and pathogenicity of biofilms of S. mutans in the context of ASC.IMPORTANCEAdult severe caries (ASC), as a special type of acute caries, is rarely reported and its worthiness of further study is still in dispute. Yet studies on the etiology of severe caries in adults have not found a clear pathogenic mechanism for it. Knowledge of the oral microbiota is important for the treatment of dental caries. We discovered that the interaction between V. parvula and S. mutans augments the severity of dental caries in vivo, suggesting V. parvula may act as a synergistic pathobiont exacerbating biofilm virulence of S. mutans in ASC. Our findings may improve the understanding of ASC pathogenesis and are likely to provide a basis for planning appropriate therapeutic strategies.
期刊介绍:
Microbiology Spectrum publishes commissioned review articles on topics in microbiology representing ten content areas: Archaea; Food Microbiology; Bacterial Genetics, Cell Biology, and Physiology; Clinical Microbiology; Environmental Microbiology and Ecology; Eukaryotic Microbes; Genomics, Computational, and Synthetic Microbiology; Immunology; Pathogenesis; and Virology. Reviews are interrelated, with each review linking to other related content. A large board of Microbiology Spectrum editors aids in the development of topics for potential reviews and in the identification of an editor, or editors, who shepherd each collection.