scholarly journals Diversity in Antagonistic Interactions between Commensal Oral Streptococci and Streptococcus mutans

2017 ◽  
Vol 52 (1-2) ◽  
pp. 88-101 ◽  
Author(s):  
Xuelian Huang ◽  
Christopher M. Browngardt ◽  
Min Jiang ◽  
Sang-Joon Ahn ◽  
Robert A. Burne ◽  
...  

Arginine metabolism via the arginine deiminase system (ADS) of oral bacteria generates ammonia, which can increase the pH of oral biofilms and decrease the risk for dental caries. Antagonistic interactions between ADS-positive and cariogenic bacteria in oral biofilms may be an important ecological determinant of caries. This study investigated the antagonistic potential and mechanisms of clinical isolates of arginolytic streptococci on and by Streptococcus mutans UA159, a well-characterized cariogenic human isolate. Low-passage isolates of Streptococcus gordonii, Streptococcus sanguinis, Streptococcus parasanguinis, Streptococcus australis, and Streptococcus cristatus inhibited the growth of S. mutans to various degrees when they were inoculated on growth media first or simultaneously with S. mutans. The antagonistic effects of arginolytic strains against S. mutans and the production of H2O2 by these strains were enhanced during growth in a less-rich medium or when galactose was substituted for glucose as the primary carbohydrate source. Pyruvate oxidase was the dominant pathway for H2O2 production by arginolytic strains, but lactate oxidase activity was also detected in some strains of S. gordonii and S. cristatus. UA159 inhibited the growth of all tested arginolytic strains when inoculated first, especially in aerobic conditions. However, the antagonistic effects of S. mutans on certain strains of S. gordonii and S. australis were not observed during anaerobic growth in the presence of arginine. Thus, arginolytic commensal streptococci may have a synergistically positive impact on the ecology of oral biofilms by moderating biofilm pH while antagonizing the growth and virulence of caries pathogens.

2008 ◽  
Vol 190 (13) ◽  
pp. 4632-4640 ◽  
Author(s):  
Jens Kreth ◽  
Yongshu Zhang ◽  
Mark C. Herzberg

ABSTRACT Biofilms are polymicrobial, with diverse bacterial species competing for limited space and nutrients. Under healthy conditions, the different species in biofilms maintain an ecological balance. This balance can be disturbed by environmental factors and interspecies interactions. These perturbations can enable dominant growth of certain species, leading to disease. To model clinically relevant interspecies antagonism, we studied three well-characterized and closely related oral species, Streptococcus gordonii, Streptococcus sanguinis, and cariogenic Streptococcus mutans. S. sanguinis and S. gordonii used oxygen availability and the differential production of hydrogen peroxide (H2O2) to compete effectively against S. mutans. Interspecies antagonism was influenced by glucose with reduced production of H2O2. Furthermore, aerobic conditions stimulated the competence system and the expression of the bacteriocin mutacin IV of S. mutans, as well as the H2O2-dependent release of heterologous DNA from mixed cultures of S. sanguinis and S. gordonii. These data provide new insights into ecological factors that determine the outcome of competition between pioneer colonizing oral streptococci and the survival mechanisms of S. mutans in the oral biofilm.


2020 ◽  
Vol 202 (12) ◽  
Author(s):  
Delphine Dufour ◽  
Abdelahhad Barbour ◽  
Yuki Chan ◽  
Marcus Cheng ◽  
Taimoor Rahman ◽  
...  

ABSTRACT Bacteriocins are ribosomally synthesized proteinaceous antibacterial peptides. They selectively interfere with the growth of other bacteria. The production and secretion of bacteriocins confer a distinct ecological advantage to the producer in competing against other bacteria that are present in the same ecological niche. Streptococcus mutans, a significant contributor to the development of dental caries, is one of the most prolific producers of bacteriocins, known as mutacins in S. mutans. In this study, we characterized the locus encoding mutacin B-Ny266, a lantibiotic with a broad spectrum of activity. The chromosomal locus is composed of six predicted operon structures encoding proteins involved in regulation, antimicrobial activity, biosynthesis, modification, transport, and immunity. Mutacin B-Ny266 was purified from semisolid cultures, and two inhibitory peptides, LanA and LanA′, were detected. Both peptides were highly modified. Such modifications include dehydration of serine and threonine and the formation of a C-terminal aminovinyl-cysteine (AviCys) ring. While LanA peptide alone is absolutely required for antimicrobial activity, the presence of LanA′ enhanced the activity of LanA, suggesting that B-Ny266 may function as a two-peptide lantibiotic. The activation of lanAA′ expression is most likely controlled by the conserved two-component system NsrRS, which is activated by LanA peptide but not by LanA′. The chromosomal locus encoding mutacin B-Ny266 was not universally conserved in all sequenced S. mutans genomes. Intriguingly, the genes encoding LanAA′ peptides were restricted to the most invasive serotypes of S. mutans. IMPORTANCE Although dental caries is largely preventable, it remains the most common and costly infectious disease worldwide. Caries is initiated by the presence of dental plaque biofilm that contains Streptococcus mutans, a species extensively characterized by its role in caries development and formation. S. mutans deploys an arsenal of strategies to establish itself within the oral cavity. One of them is the production of bacteriocins that confer a competitive advantage by targeting and killing closely related competitors. In this work, we found that mutacin B-Ny266 is a potent lantibiotic that is effective at killing a wide array of oral streptococci, including nearly all S. mutans strains tested. Lantibiotics produced by oral bacteria could represent a promising strategy to target caries pathogens embedded in dental plaque biofilm.


2019 ◽  
Author(s):  
Lulu Chen ◽  
Brinta Chakraborty ◽  
Jing Zou ◽  
Robert A. Burne ◽  
Lin Zeng

ABSTRACTN-acetylglucosamine (GlcNAc) and glucosamine (GlcN) enhance the competitiveness of the laboratory strain DL1 ofStreptococcus gordoniiagainst the caries pathogenStreptococcus mutans. Here we examine how amino sugars affect the interaction of five low-passage clinical isolates of abundant commensal streptococci withS. mutansutilizing a dual-species biofilm model. Compared to glucose, growth on GlcN or GlcNAc significantly reduced the viability ofS. mutansin co-cultures with most commensals, shifting the proportions of species. Consistent with these results, production of H2O2was increased in most commensals when growing on amino sugars, and inhibition ofS. mutansbyStreptococcus cristatus, Streptococcus oralis,orS. gordoniiwas enhanced by amino sugars on agar plates. All commensals exceptS. oralishad higher arginine deiminase activities when grown on GlcN, and in some cases GlcNAc. Inex vivobiofilms formed using pooled cell-containing saliva (CCS), the proportions ofS. mutanswere drastically diminished when GlcNAc was the primary carbohydrate. Increased production of H2O2could account in large part for the inhibitory effects of CCS biofilms. Surprisingly, amino sugars appeared to improve mutacin production byS. mutanson agar plates, suggesting that the commensals have mechanisms to actively subvert antagonism byS. mutansin co-cultures. Collectively, these findings demonstrate that amino sugars can enhance the beneficial properties of low-passage commensal oral streptococci and highlight their potential for moderating the cariogenicity of oral biofilms.SIGNIFICANCEDental caries is driven by dysbiosis of oral biofilms in which dominance by acid-producing and acid-tolerant bacteria results in loss of tooth mineral. Our previous work demonstrated the beneficial effects of amino sugars, GlcNAc and GlcN, in promoting the antagonistic properties of a health-associated oral bacterium,Streptococcus gordonii,in competition with the major caries pathogenStreptococcus mutans.Here we investigated 5 low-passage clinical isolates of the most common streptococcal species to establish how amino sugars may influence the ecology and virulence of oral biofilms. Using multiplein vitromodels, including a human saliva-derived microcosm biofilm, experiments showed significant enhancement by at least one amino sugar in the ability of most of these bacteria to suppress the caries pathogen. Therefore, our findings demonstrated the mechanism of action by which amino sugars may affect human oral biofilms to promote health.


2019 ◽  
Vol 85 (10) ◽  
Author(s):  
Lulu Chen ◽  
Brinta Chakraborty ◽  
Jing Zou ◽  
Robert A. Burne ◽  
Lin Zeng

ABSTRACTN-Acetylglucosamine (GlcNAc) and glucosamine (GlcN) enhance the competitiveness of the laboratory strain DL1 ofStreptococcus gordoniiagainst the caries pathogenStreptococcus mutans. Here, we examine how amino sugars affect the interaction of five low-passage-number clinical isolates of abundant commensal streptococci withS. mutansby utilizing a dual-species biofilm model. Compared to that for glucose, growth on GlcN or GlcNAc significantly reduced the viability ofS. mutansin cocultures with most commensals, shifting the proportions of species. Consistent with these results, production of H2O2was increased in most commensals when growing on amino sugars, and inhibition ofS. mutansbyStreptococcus cristatus,Streptococcus oralis, orS. gordoniiwas enhanced by amino sugars on agar plates. All commensals exceptS. oralishad higher arginine deiminase activities when grown on GlcN and, in some cases, GlcNAc. Inex vivobiofilms formed using pooled cell-containing saliva (CCS), the proportions ofS. mutanswere drastically diminished when GlcNAc was the primary carbohydrate. Increased production of H2O2could account in large part for the inhibitory effects of CCS biofilms. Surprisingly, amino sugars appeared to improve mutacin production byS. mutanson agar plates, suggesting that the commensals have mechanisms to actively subvert antagonism byS. mutansin cocultures. Collectively, these findings demonstrate that amino sugars can enhance the beneficial properties of low-passage-number commensal oral streptococci and highlight their potential for moderating the cariogenicity of oral biofilms.IMPORTANCEDental caries is driven by dysbiosis of oral biofilms in which dominance by acid-producing and acid-tolerant bacteria results in loss of tooth mineral. Our previous work demonstrated the beneficial effects of amino sugars GlcNAc and GlcN in promoting the antagonistic properties of a health-associated oral bacterium,Streptococcus gordonii, in competition with the major caries pathogenStreptococcus mutans. Here, we investigated 5 low-passage-number clinical isolates of the most common streptococcal species to establish how amino sugars may influence the ecology and virulence of oral biofilms. Using multiplein vitromodels, including a human saliva-derived microcosm biofilm, experiments showed significant enhancement by at least one amino sugar in the ability of most of these bacteria to suppress the caries pathogen. Therefore, our findings demonstrated the mechanism of action by which amino sugars may affect human oral biofilms to promote health.


2016 ◽  
Vol 82 (12) ◽  
pp. 3671-3682 ◽  
Author(s):  
Lin Zeng ◽  
Tanaz Farivar ◽  
Robert A. Burne

ABSTRACTBiochemical and genetic aspects of the metabolism of the amino sugarsN-acetylglucosamine (GlcNAc) and glucosamine (GlcN) by commensal oral streptococci and the effects of these sugars on interspecies competition with the dental caries pathogenStreptococcus mutanswere explored. MultipleS. mutanswild-type isolates displayed long lag phases when transferred from glucose-containing medium to medium with GlcNAc as the primary carbohydrate source, but commensal streptococci did not. Competition in liquid coculture or dual-species biofilms betweenS. mutansandStreptococcus gordoniishowed thatS. gordoniiwas particularly dominant when the primary carbohydrate was GlcN or GlcNAc. Transcriptional and enzymatic assays showed that the catabolic pathway for GlcNAc was less highly induced inS. mutansthan inS. gordonii. Exposure to H2O2, which is produced byS. gordoniiand antagonizes the growth ofS. mutans, led to reduced mRNA levels ofnagAandnagBinS. mutans. When the gene for the transcriptional regulatory NagR was deleted inS. gordonii, the strain produced constitutively high levels ofnagA(GlcNAc-6-P deacetylase),nagB(GlcN-6-P deaminase), andglmS(GlcN-6-P synthase) mRNA. Similar to NagR ofS. mutans(NagRSm), theS. gordoniiNagR protein (NagRSg) could bind to consensus binding sites (dre) in thenagA,nagB, andglmSpromoter regions ofS. gordonii. Notably, NagRSgbinding was inhibited by GlcN-6-P, but G-6-P had no effect, unlike for NagRSm. This study expands the understanding of amino sugar metabolism and NagR-dependent gene regulation in streptococci and highlights the potential for therapeutic applications of amino sugars to prevent dental caries.IMPORTANCEAmino sugars are abundant in the biosphere, so the relative efficiency of particular bacteria in a given microbiota to metabolize these sources of carbon and nitrogen might have a profound impact on the ecology of the community. Our investigation reveals that several oral commensal bacteria have a much greater capacity to utilize amino sugars than the dental pathogenStreptococcus mutansand that the ability of the model commensalStreptococcus gordoniito compete againstS. mutansis substantively enhanced by the presence of amino sugars commonly found in the oral cavity. The mechanisms underlying the greater capacity and competitive enhancements of the commensal are shown to depend on how the genes for the catabolic enzymes are regulated, the role of the allosteric modulators affecting such regulation, and the ability of amino sugars to enhance certain activities of the commensal that are antagonistic toS. mutans.


2005 ◽  
Vol 71 (1) ◽  
pp. 354-362 ◽  
Author(s):  
Bing-Yan Wang ◽  
Howard K. Kuramitsu

ABSTRACT Streptococcus mutans has been recognized as an important etiological agent in human dental caries. Some strains of S. mutans also produce bacteriocins. In this study, we sought to demonstrate that bacteriocin production by S. mutans strains GS5 and BM71 was mediated by quorum sensing, which is dependent on a competence-stimulating peptide (CSP) signaling system encoded by the com genes. We also demonstrated that interactions with some other oral streptococci interfered with S. mutans bacteriocin production both in broth and in biofilms. The inhibition of S. mutans bacteriocin production by oral bacteria was stronger in biofilms than in broth. Using transposon Tn916 mutagenesis, we identified a gene (sgc; named for Streptococcus gordonii challisin) responsible for the inhibition of S. mutans bacteriocin production by S. gordonii Challis. Interruption of the sgc gene in S. gordonii Challis resulted in attenuated inhibition of S. mutans bacteriocin production. The supernatant fluids from the sgc mutant did not inactivate the exogenous S. mutans CSP as did those from the parent strain Challis. S. gordonii Challis did not inactivate bacteriocin produced by S. mutans GS5. Because S. mutans uses quorum sensing to regulate virulence, strategies designed to interfere with these signaling systems may have broad applicability for biological control of this caries-causing organism.


1999 ◽  
Vol 67 (4) ◽  
pp. 1878-1886 ◽  
Author(s):  
Michael F. Cole ◽  
Stacey Bryan ◽  
Mishell K. Evans ◽  
Cheryl L. Pearce ◽  
Michael J. Sheridan ◽  
...  

ABSTRACT Secretory immunoglobulin A (SIgA) antibodies reactive with the pioneer oral streptococci Streptococcus mitis biovar 1 andStreptococcus oralis, the late oral colonizerStreptococcus mutans, and the pioneer enteric bacteriumEnterococcus faecalis in saliva samples from 10 human infants from birth to age 2 years were analyzed. Low levels of salivary SIgA1 and SIgA2 antibodies reactive with whole cells of all four species were detected within the first month after birth, even thoughS. mutans and E. faecalis were not recovered from the mouths of the infants during the study period. Although there was a fivefold increase in the concentration of SIgA between birth and age 2 years, there were no differences between the concentrations of SIgA1 and SIgA2 antibodies reactive with the four species over this time period. When the concentrations of SIgA1 and SIgA2 antibodies reactive with all four species were normalized to the concentrations of SIgA1 and SIgA2 in saliva, SIgA1 and SIgA2 antibodies reactive with these bacteria showed a significant decrease from birth to 2 years of age. Adsorption of each infant’s saliva with cells of one species produced a dramatic reduction of antibodies recognizing the other three species. Sequential adsorption of saliva samples removed all SIgA antibody to the bacteria, indicating that the SIgA antibodies were directed to antigens shared by all four species. The induction by the host of a limited immune response to common antigens that are likely not involved in adherence may be among the mechanisms that commensal streptococci employ to persist in the oral cavity.


2001 ◽  
Vol 183 (20) ◽  
pp. 6074-6084 ◽  
Author(s):  
José A. C. Lemos ◽  
Yi-Ywan M. Chen ◽  
Robert A. Burne

ABSTRACT Our working hypothesis is that the major molecular chaperones DnaK and GroE play central roles in the ability of oral bacteria to cope with the rapid and frequent stresses encountered in oral biofilms, such as acidification and nutrient limitation. Previously, our laboratory partially characterized the dnaK operon ofStreptococcus mutans(hrcA-grpE-dnaK) and demonstrated that dnaK is up-regulated in response to acid shock and sustained acidification (G. C. Jayaraman, J. E. Penders, and R. A. Burne, Mol. Microbiol. 25:329–341, 1997). Here, we show that thegroESL genes of S. mutans constitute an operon that is expressed from a stress-inducible ςA-type promoter located immediately upstream of a CIRCE element. GroEL protein and mRNA levels were elevated in cells exposed to a variety of stresses, including acid shock. A nonpolar insertion into hrcA was created and used to demonstrate that HrcA negatively regulates the expression of thegroEL and dnaK operons. The SM11 mutant, which had constitutively high levels of GroESL and roughly 50% of the DnaK protein found in the wild-type strain, was more sensitive to acid killing and could not lower the pH as effectively as the parent. The acid-sensitive phenotype of SM11 was, at least in part, attributable to lower F1F0-ATPase activity. A minimum of 10 proteins, in addition to GroES-EL, were found to be up-regulated in SM11. The data clearly indicate that HrcA plays a key role in the regulation of chaperone expression in S. mutans and that changes in the levels of the chaperones profoundly influence acid tolerance.


2000 ◽  
Vol 182 (5) ◽  
pp. 1374-1382 ◽  
Author(s):  
C. Y. Loo ◽  
D. A. Corliss ◽  
N. Ganeshkumar

ABSTRACT Viridans streptococci, which include Streptococcus gordonii, are pioneer oral bacteria that initiate dental plaque formation. Sessile bacteria in a biofilm exhibit a mode of growth that is distinct from that of planktonic bacteria. Biofilm formation ofS. gordonii Challis was characterized using an in vitro biofilm formation assay on polystyrene surfaces. The same assay was used as a nonbiased method to screen isogenic mutants generated by Tn916 transposon mutagenesis for defective biofilm formation. Biofilms formed optimally when bacteria were grown in a minimal medium under anaerobic conditions. Biofilm formation was affected by changes in pH, osmolarity, and carbohydrate content of the growth media. Eighteen biofilm-defective mutants ofS. gordonii Challis were identified based on Southern hybridization with a Tn916-based probe and DNA sequences of the Tn916-flanking regions. Molecular analyses of these mutants showed that some of the genes required for biofilm formation are involved in signal transduction, peptidoglycan biosynthesis, and adhesion. These characteristics are associated with quorum sensing, osmoadaptation, and adhesion functions in oral streptococci. Only nine of the biofilm-defective mutants had defects in genes of known function, suggesting that novel aspects of bacterial physiology may play a part in biofilm formation. Further identification and characterization of biofilm-associated genes will provide insight into the molecular mechanisms of biofilm formation of oral streptococci.


2021 ◽  
Author(s):  
Madeline Krieger ◽  
Justin Merritt ◽  
Rahul Raghavan

Streptococcus mutans is a major pathobiont involved in the development of dental caries. Its ability to utilize numerous sugars and to effectively respond to environmental stress promotes S. mutans proliferation in oral biofilms. Because of their quick action and low energetic cost, non-coding small RNAs (sRNAs) represent an ideal mode of gene regulation in stress response networks, yet their roles in oral pathogens have remained largely unexplored. We identified 15 novel sRNAs in S. mutans and show that they respond to four stress-inducing conditions commonly encountered by the pathogen in human mouth: sugar-phosphate stress, hydrogen peroxide exposure, high temperature, and low pH. To better understand the role of sRNAs in S. mutans, we further explored the function of the novel sRNA, SmsR4. Our data demonstrate that SmsR4 regulates the EIIA component of the sorbitol phosphotransferase system, which transports and phosphorylates the sugar alcohol sorbitol. The fine-tuning of EIIA availability by SmsR4 likely promotes S. mutans growth while using sorbitol as the main carbon source. Our work lays a foundation for understanding the role of sRNAs in regulating gene expression in stress response networks in S. mutans and highlights the importance of the underexplored phenomenon of posttranscriptional gene regulation in oral bacteria.


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