Literature DB >> 30877119

Amino Sugars Modify Antagonistic Interactions between Commensal Oral Streptococci and Streptococcus mutans.

Lulu Chen1,2, Brinta Chakraborty2, Jing Zou1, Robert A Burne2, Lin Zeng3.   

Abstract

N-Acetylglucosamine (GlcNAc) and glucosamine (GlcN) enhance the competitiveness of the laboratory strain DL1 of Streptococcus gordonii against the caries pathogen Streptococcus mutans Here, we examine how amino sugars affect the interaction of five low-passage-number clinical isolates of abundant commensal streptococci with S. mutans by utilizing a dual-species biofilm model. Compared to that for glucose, growth on GlcN or GlcNAc significantly reduced the viability of S. mutans in cocultures with most commensals, shifting the proportions of species. Consistent with these results, production of H2O2 was increased in most commensals when growing on amino sugars, and inhibition of S. mutans by Streptococcus cristatus, Streptococcus oralis, or S. gordonii was enhanced by amino sugars on agar plates. All commensals except S. oralis had higher arginine deiminase activities when grown on GlcN and, in some cases, GlcNAc. In ex vivo biofilms formed using pooled cell-containing saliva (CCS), the proportions of S. mutans were drastically diminished when GlcNAc was the primary carbohydrate. Increased production of H2O2 could account in large part for the inhibitory effects of CCS biofilms. Surprisingly, amino sugars appeared to improve mutacin production by S. mutans on agar plates, suggesting that the commensals have mechanisms to actively subvert antagonism by S. mutans in 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.IMPORTANCE Dental 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 pathogen Streptococcus 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 multiple in vitro models, 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.
Copyright © 2019 American Society for Microbiology.

Entities:  

Keywords:  Streptococcus mutans; amino sugars; bacterial antagonism; clinical commensal isolates; hydrogen peroxide

Year:  2019        PMID: 30877119      PMCID: PMC6498165          DOI: 10.1128/AEM.00370-19

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  59 in total

1.  The effect of inoculum source and fluid shear force on the development of in vitro oral multispecies biofilms.

Authors:  C E Fernández; M B Aspiras; M W Dodds; C González-Cabezas; A H Rickard
Journal:  J Appl Microbiol       Date:  2017-03       Impact factor: 3.772

2.  Differential oxidative stress tolerance of Streptococcus mutans isolates affects competition in an ecological mixed-species biofilm model.

Authors:  Yuan Liu; Sara R Palmer; Hsiaochi Chang; Ashton N Combs; Robert A Burne; Hyun Koo
Journal:  Environ Microbiol Rep       Date:  2017-12-04       Impact factor: 3.541

3.  Diversity in Antagonistic Interactions between Commensal Oral Streptococci and Streptococcus mutans.

Authors:  Xuelian Huang; Christopher M Browngardt; Min Jiang; Sang-Joon Ahn; Robert A Burne; Marcelle M Nascimento
Journal:  Caries Res       Date:  2017-12-20       Impact factor: 4.056

4.  Amino Sugars Enhance the Competitiveness of Beneficial Commensals with Streptococcus mutans through Multiple Mechanisms.

Authors:  Lin Zeng; Tanaz Farivar; Robert A Burne
Journal:  Appl Environ Microbiol       Date:  2016-05-31       Impact factor: 4.792

5.  Phenotypic differentiation of Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus strains within the "Streptococcus milleri group".

Authors:  R A Whiley; H Fraser; J M Hardie; D Beighton
Journal:  J Clin Microbiol       Date:  1990-07       Impact factor: 5.948

6.  Biofilm formation and virulence expression by Streptococcus mutans are altered when grown in dual-species model.

Authors:  Zezhang T Wen; David Yates; Sang-Joon Ahn; Robert A Burne
Journal:  BMC Microbiol       Date:  2010-04-14       Impact factor: 3.605

Review 7.  Acid-adaptive mechanisms of Streptococcus mutans-the more we know, the more we don't.

Authors:  J L Baker; R C Faustoferri; R G Quivey
Journal:  Mol Oral Microbiol       Date:  2016-06-21       Impact factor: 3.563

8.  Evaluation of the capacity of oral streptococci to produce hydrogen peroxide.

Authors:  A García-Mendoza; J Liébana; A M Castillo; A de la Higuera; G Piédrola
Journal:  J Med Microbiol       Date:  1993-12       Impact factor: 2.472

Review 9.  Progress toward understanding the contribution of alkali generation in dental biofilms to inhibition of dental caries.

Authors:  Ya-Ling Liu; Marcelle Nascimento; Robert A Burne
Journal:  Int J Oral Sci       Date:  2012-09-21       Impact factor: 6.344

10.  L-arginine destabilizes oral multi-species biofilm communities developed in human saliva.

Authors:  Ethan Kolderman; Deepti Bettampadi; Derek Samarian; Scot E Dowd; Betsy Foxman; Nicholas S Jakubovics; Alexander H Rickard
Journal:  PLoS One       Date:  2015-05-06       Impact factor: 3.240

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  13 in total

1.  Novel Probiotic Mechanisms of the Oral Bacterium Streptococcus sp. A12 as Explored with Functional Genomics.

Authors:  K Lee; A R Walker; B Chakraborty; J R Kaspar; M M Nascimento; R A Burne
Journal:  Appl Environ Microbiol       Date:  2019-10-16       Impact factor: 4.792

2.  [Design, screening and antimicrobial activity of novel peptides against Streptococcus mutans].

Authors:  Dongsheng Liang; Huanying Li; Xiaohu Xu; Jingheng Liang; Xingzhu Dai; Wanghong Zhao
Journal:  Nan Fang Yi Ke Da Xue Xue Bao       Date:  2019-07-30

3.  Microbial Interactions in Oral Communities Mediate Emergent Biofilm Properties.

Authors:  P I Diaz; A M Valm
Journal:  J Dent Res       Date:  2019-10-07       Impact factor: 6.116

4.  Spontaneously Arising Streptococcus mutans Variants with Reduced Susceptibility to Chlorhexidine Display Genetic Defects and Diminished Fitness.

Authors:  Justin R Kaspar; Matthew J Godwin; Irina M Velsko; Vincent P Richards; Robert A Burne
Journal:  Antimicrob Agents Chemother       Date:  2019-06-24       Impact factor: 5.191

5.  Spontaneous Mutants of Streptococcus sanguinis with Defects in the Glucose-Phosphotransferase System Show Enhanced Post-Exponential-Phase Fitness.

Authors:  Lin Zeng; Alejandro R Walker; Kyulim Lee; Zachary A Taylor; Robert A Burne
Journal:  J Bacteriol       Date:  2021-08-30       Impact factor: 3.490

6.  Amino Sugars Reshape Interactions between Streptococcus mutans and Streptococcus gordonii.

Authors:  Lulu Chen; Alejandro R Walker; Robert A Burne; Lin Zeng
Journal:  Appl Environ Microbiol       Date:  2020-12-17       Impact factor: 4.792

7.  Regulatory circuits controlling Spx levels in Streptococcus mutans.

Authors:  Tridib Ganguly; Jessica K Kajfasz; Jacqueline Abranches; José A Lemos
Journal:  Mol Microbiol       Date:  2020-04-08       Impact factor: 3.501

8.  Precision targeting of bacterial pathogen via bi-functional nanozyme activated by biofilm microenvironment.

Authors:  Yue Huang; Yuan Liu; Shrey Shah; Dongyeop Kim; Aurea Simon-Soro; Tatsuro Ito; Maryam Hajfathalian; Yong Li; Jessica C Hsu; Lenitza M Nieves; Faizan Alawi; Pratap C Naha; David P Cormode; Hyun Koo
Journal:  Biomaterials       Date:  2020-11-27       Impact factor: 12.479

9.  A single system detects and protects the beneficial oral bacterium Streptococcus sp. A12 from a spectrum of antimicrobial peptides.

Authors:  Kyulim Lee; Justin R Kaspar; Gisela Rojas-Carreño; Alejandro R Walker; Robert A Burne
Journal:  Mol Microbiol       Date:  2021-02-25       Impact factor: 3.979

10.  Subpopulation behaviors in lactose metabolism by Streptococcus mutans.

Authors:  Lin Zeng; Robert A Burne
Journal:  Mol Microbiol       Date:  2020-10-06       Impact factor: 3.501

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