TetR Family Regulator brpT Modulates Biofilm Formation in Streptococcus sanguinis

Liu, Jinlin; Stone, Victoria; Ge, Xuming; Tang, Madison; El-Rami, Fadi; Xu, Ping

doi:10.1371/journal.pone.0169301

Cited by 15 publications

(23 citation statements)

References 51 publications

(59 reference statements)

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“…disruptions in biofilm formation or structure result in attenuation of virulence (48,49). To determine whether there is a link between biofilms and virulence among the additional S. sanguinis strains in our collection, strains were grown in biofilm medium supplemented with either sucrose (50) or glucose (51) to model oral (52,53) and cardiac conditions, respectively. As shown in Fig.…”

Section: Figmentioning

confidence: 99%

Genomic, Phenotypic, and Virulence Analysis of Streptococcus sanguinis Oral and Infective-Endocarditis Isolates

2019

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Streptococcus sanguinis, an abundant and benign inhabitant of the oral cavity, is an important etiologic agent of infective endocarditis (IE), particularly in people with predisposing cardiac valvular damage. Although commonly isolated from patients with IE, little is known about the factors that make any particular S. sanguinis isolate more virulent than another or, indeed, whether significant differences in virulence exist among isolates. In this study, we compared the genomes of a collection of S. sanguinis strains comprised of both oral isolates and bloodstream isolates from patients diagnosed with IE. Oral and IE isolates could not be distinguished by phylogenetic analyses, and we did not succeed in identifying virulence genes unique to the IE strains. We then investigated the virulence of these strains in a rabbit model of IE using a variation of the Bar-seq (barcode sequencing) method wherein we pooled the strains and used Illumina sequencing to count unique barcodes that had been inserted into each isolate at a conserved intergenic region. After we determined that several of the genome sequences were misidentified in GenBank, our virulence results were used to inform our bioinformatic analyses, identifying genes that may explain the heterogeneity in virulence. We further characterized these strains by assaying for phenotypes potentially contributing to virulence. Neither strain competition via bacteriocin production nor biofilm formation showed any apparent relationship with virulence. Increased cell-associated manganese was, however, correlated with blood isolates. These results, combined with additional phenotypic assays, suggest that S. sanguinis virulence is highly variable and results from multiple genetic factors.

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Section: Figmentioning

confidence: 99%

Genomic, Phenotypic, and Virulence Analysis of Streptococcus sanguinis Oral and Infective-Endocarditis Isolates

2019

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“…The initial step in biofilm development is attachment, followed by micro-colony formation of newly attached cells through growth expansion. This process then leads into a series of ordered and temporal events, in which coadhesion predominates, ultimately biofilm, the biofilm formed by the brpT mutant was thicker, more robust, and with a higher glucan content (44). By modulating levels of glucan synthesis, BrpT may therefore control switching of S. sanguinis biofilms from an adherent to a dissemination state.…”

Section: S Sanguinis In Biofilm Formationmentioning

confidence: 99%

Genetics ofsanguinis-Group Streptococci in Health and Disease

Nobbs

Kreth

2019

Microbiol Spectr

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With the application of increasingly advanced “omics” technologies to the study of our resident oral microbiota, the presence of a defined, health-associated microbial community has been recognized. Within this community, sanguinis -group streptococci, comprising the closely related Streptococcus sanguinis and Streptococcus gordonii , together with Streptococcus parasanguinis , often predominate. Their ubiquitous and abundant nature reflects the evolution of these bacteria as highly effective colonizers of the oral cavity. Through interactions with host tissues and other microbes, and the capacity to readily adapt to prevailing environmental conditions, sanguinis -group streptococci are able to shape accretion of the oral plaque biofilm and promote development of a microbial community that exists in harmony with its host. Nonetheless, upon gaining access to the blood stream, those very same colonization capabilities can confer upon sanguinis -group streptococci the ability to promote systemic disease. This article focuses on the role of sanguinis -group streptococci as the commensurate commensals, highlighting those aspects of their biology that enable the coordination of health-associated biofilm development. This includes the molecular mechanisms, both synergistic and antagonistic, that underpin adhesion to substrata, intercellular communication, and polymicrobial community formation. As our knowledge of these processes advances, so will the opportunities to exploit this understanding for future development of novel strategies to control oral and extraoral disease.

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“…Glucosyltransferases (GTFs) are important in sucrose induced plaque formation ( Rölla et al, 1985 ). When using sucrose as the carbon source, GtfP, the only GTF present in S. sanguinis , is responsible for glucan synthesis and essential for biofilm formation in S. sanguinis ( Yoshida et al, 2014 ; Liu et al, 2017 ). The overexpression of the gtfP gene promotes the production of water-insoluble glucan (WIG) and water-soluble glucan (WSG), which aids biofilm formation ( Yoshida et al, 2014 ; Liu et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

“…When using sucrose as the carbon source, GtfP, the only GTF present in S. sanguinis , is responsible for glucan synthesis and essential for biofilm formation in S. sanguinis ( Yoshida et al, 2014 ; Liu et al, 2017 ). The overexpression of the gtfP gene promotes the production of water-insoluble glucan (WIG) and water-soluble glucan (WSG), which aids biofilm formation ( Yoshida et al, 2014 ; Liu et al, 2017 ). Transcription of gtfP is repressed by an increase in the expression of the arginine ( arg ) biosynthesis gene ( Zhu et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

“…It has been shown that a Δ ciaR mutant with reduced gtfP expression produces less extracellular glucan resulting in deficient biofilm formation ( Zhu et al, 2017 ). Conversely, the deletion of another transcription regulator, brpT (Biofilm Regulatory Protein TetR), in S. sanguinis , promotes biofilm formation by up-regulating the transcription of gtfP , in turn generating more glucan ( Liu et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

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A Novel Regulator Modulates Glucan Production, Cell Aggregation and Biofilm Formation in Streptococcus sanguinis SK36

et al. 2018

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Streptococcus sanguinis is an early colonizer of tooth surfaces and a key player in plaque biofilm development. However, the mechanism of biofilm formation of S. sanguinis is still unclear. Here, we showed that deletion of a transcription factor, brpL, promotes cell aggregation and biofilm formation in S. sanguinis SK36. Glucan, a polysaccharide synthesized from sucrose, was over-produced and aggregated in the biofilm of ΔbrpL, which was necessary for better biofilm formation ability of ΔbrpL. Quantitative RT-PCR demonstrated that gtfP was significantly up-regulated in ΔbrpL, which increased the productions of water-insoluble and water-soluble glucans. The ΔbrpLΔgtfP double mutant decreased biofilm formation ability of ΔbrpL to a level similar like that of ΔgtfP. Interestingly, the biofilm of ΔbrpL had an increased tolerance to ampicillin treatment, which might be due to better biofilm formation ability through the mechanisms of cellular and glucan aggregation. RNA sequencing and quantitative RT-PCR revealed the modulation of a group of genes in ΔbrpL was mediated by activating the expression of ciaR, another gtfP-related biofilm formation regulator. Double deletion of brpL and ciaR decreased biofilm formation ability to the phenotype of a ΔciaR mutant. Additionally, RNA sequencing elucidated a broad range of genes, related to carbohydrate metabolism and uptake, were activated in ΔbrpL. SSA_0222, a gene involved in the phosphotransferase system, was dramatically up-regulated in ΔbrpL and essential for S. sanguinis survival under our experimental conditions. In summary, brpL modulates glucan production, cell aggregation and biofilm formation by regulating the expression of ciaR in S. sanguinis SK36.

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TetR Family Regulator brpT Modulates Biofilm Formation in Streptococcus sanguinis

Cited by 15 publications

References 51 publications

Genomic, Phenotypic, and Virulence Analysis of Streptococcus sanguinis Oral and Infective-Endocarditis Isolates

Genomic, Phenotypic, and Virulence Analysis of Streptococcus sanguinis Oral and Infective-Endocarditis Isolates

Genetics ofsanguinis-Group Streptococci in Health and Disease

A Novel Regulator Modulates Glucan Production, Cell Aggregation and Biofilm Formation in Streptococcus sanguinis SK36

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