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      Understanding LrgAB Regulation of Streptococcus mutans Metabolism

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          Abstract

          Lack of LrgAB renders cariogenic Streptococcus mutans more sensitive to oxidative stress, as well as limits the capacity of this organism to re-uptake pyruvate upon starvation. This study was aimed at investigating the ecological and metabolic contribution of LrgAB to competitive fitness, using S. mutans strains, that either lack or overexpress lrgAB. These experiments revealed that impaired aerobic growth of the Δ lrgAB mutant can be effectively restored by supplementation of pyruvate, and that perturbated expression of lrgAB significantly affects pyruvate flux and the conversion of pyruvate to acetyl-CoA by the Pdh pathway, verifying that LrgAB is closely linked to pyruvate catabolism. In vitro competition assays revealed that LrgAB plays an important role in S. mutans competition with H 2O 2-producing S. gordonii, an interaction which can also be modulated by external pyruvate. However, no obvious competitive disadvantage was observed against S. gordonii by either the S. mutans lrgAB mutant or lrgAB overexpression strain in vivo using a mouse caries model. Organic acid analysis of mouse dental biofilms revealed that metabolites produced by the host and/or dental plaque microbiota could complement the deficiency of a lrgAB mutant, and favored S. mutans establishment compared to S. gordonii. Collectively, these results reinforce the importance of the oral microbiota and the metabolic environment in the oral cavity battleground, and highlight that pyruvate uptake through LrgAB may be crucial for interspecies competition that drives niche occupancy.

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          The exopolysaccharide matrix: a virulence determinant of cariogenic biofilm.

          Many infectious diseases in humans are caused or exacerbated by biofilms. Dental caries is a prime example of a biofilm-dependent disease, resulting from interactions of microorganisms, host factors, and diet (sugars), which modulate the dynamic formation of biofilms on tooth surfaces. All biofilms have a microbial-derived extracellular matrix as an essential constituent. The exopolysaccharides formed through interactions between sucrose- (and starch-) and Streptococcus mutans-derived exoenzymes present in the pellicle and on microbial surfaces (including non-mutans) provide binding sites for cariogenic and other organisms. The polymers formed in situ enmesh the microorganisms while forming a matrix facilitating the assembly of three-dimensional (3D) multicellular structures that encompass a series of microenvironments and are firmly attached to teeth. The metabolic activity of microbes embedded in this exopolysaccharide-rich and diffusion-limiting matrix leads to acidification of the milieu and, eventually, acid-dissolution of enamel. Here, we discuss recent advances concerning spatio-temporal development of the exopolysaccharide matrix and its essential role in the pathogenesis of dental caries. We focus on how the matrix serves as a 3D scaffold for biofilm assembly while creating spatial heterogeneities and low-pH microenvironments/niches. Further understanding on how the matrix modulates microbial activity and virulence expression could lead to new approaches to control cariogenic biofilms.
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            The mechanisms of carbon catabolite repression in bacteria.

            Carbon catabolite repression (CCR) is the paradigm of cellular regulation. CCR happens when bacteria are exposed to two or more carbon sources and one of them is preferentially utilised (frequently glucose). CCR is often mediated by several mechanisms, which can either affect the synthesis of catabolic enzymes via global or specific regulators or inhibit the uptake of a carbon source and thus the formation of the corresponding inducer. The major CCR mechanisms operative in Enterobacteriaceae and Firmicutes are quite different, but in both types of organisms components of the phosphoenolpyruvate:carbohydrate phosphotransferase system (PTS) and protein phosphorylation play a major role. PTS-independent CCR mechanisms are operative in several other bacteria.
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              Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans.

              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 (H(2)O(2)) to compete effectively against S. mutans. Interspecies antagonism was influenced by glucose with reduced production of H(2)O(2). Furthermore, aerobic conditions stimulated the competence system and the expression of the bacteriocin mutacin IV of S. mutans, as well as the H(2)O(2)-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.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                03 September 2020
                2020
                : 11
                : 2119
                Affiliations
                [1] 1Department of Oral Biology, College of Dentistry, University of Florida , Gainesville, FL, United States
                [2] 2Department of Microbiology and Cell Science, Institute of Food and Agricultural Sciences, University of Florida , Gainesville, FL, United States
                Author notes

                Edited by: Ulrike Kappler, The University of Queensland, Australia

                Reviewed by: Jens Kreth, Oregon Health and Science University, United States; Marlise Inez Klein, Paulista State University, Brazil; Mingyun Li, Sichuan University, China

                *Correspondence: Sang-Joon Ahn, sahn@ 123456dental.ufl.edu

                This article was submitted to Microbial Physiology and Metabolism, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.02119
                7496758
                33013773
                a362291a-fa1e-4eee-b56f-4d9721e3d8f6
                Copyright © 2020 Ahn, Hull, Desai, Rice and Culp.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 June 2020
                : 11 August 2020
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 68, Pages: 16, Words: 0
                Funding
                Funded by: National Institute of Dental and Craniofacial Research 10.13039/100000072
                Award ID: DE025237
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                streptococcus mutans,pyruvate,lrgab,dual-species,caries,mouse model
                Microbiology & Virology
                streptococcus mutans, pyruvate, lrgab, dual-species, caries, mouse model

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