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Fructose activates a stress response shared by methylglyoxal and hydrogen peroxide in streptococcus mutans

ABSTRACT: Fructose catabolism by Streptococcus mutans is initiated by three PTS transporters yielding either fructose-1-phoshate (F-1-P) or fructose-6-phosphate (F-6-P). Deletion of one such F-1-P-generating PTS, fruI, has been shown to reduce the cariogenicity of S. mutans in rats fed a high-sucrose diet. Moreover, a recent study linked fructose metabolism in S. mutans to a reactive electrophile species (RES) methylglyoxal. Here, we conducted a comparative transcriptomic analysis of exponentially grown S. mutans shocked with 50 mM fructose, 50 mM glucose, 5 mM methylglyoxal, or 0.5 mM hydrogen peroxide (H2O2). The results revealed a striking overlap between the fructose and methylglyoxal transcriptomes, totaling 176 genes, 61 of which were also shared with the H2O2 transcriptome. This core of genes encompassed many of the same pathways affected by exposure to low pH or zinc intoxication. Consistent with these findings, fructose negatively impacted metal homeostasis of a mutant deficient in a zinc exporter and the growth of a mutant of the major oxidative stress regulator SpxA1. We further demonstrated the induction of the superoxide dismutase (sodA) and the fruRKI operon by different levels of fructose. Finally, fructose metabolism lowered culture pH at a faster pace, allowed better survival under acidic and nutrient-depleted conditions, and enhanced the competitiveness of S. mutans against Streptococcus sanguinis, although a moderated level of F-1-P might further boost some of these benefits. In conclusion, fructose metabolism is integrated into the stress core of S. mutans and regulates critical functions required for survival in both the oral cavity and during systemic infections.

ORGANISM(S): Streptococcus mutans

PROVIDER: GSE279080 | GEO | 2025/04/14

REPOSITORIES: GEO

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Project description:Candida albicans, a major opportunistic fungal pathogen is frequently found together with Streptococcus mutans in dental biofilms associated with severe childhood tooth-decay, a prevalent pediatric oral disease. Previous studies have demonstrated that S. mutans and C. albicans synergizes virulence of plaque-biofilms in vivo. However, the nature of this bacterial-fungal relationship in this cross-kingdom biofilm remains largely uncharacterized. Using iTRAQ based quantitative proteomics, we found that proteins associated with carbohydrate metabolism such as alpha-1,4 glucan phosphorylase, Hexokinase-2, Isocitrate lyase and malate synthase were significantly upregulated in C. albicans in the mixed-species biofilms (P<0.05). C. albicans proteins associated with growth/morphogenesis such as pH-responsive protein-2, Fma1p and Hsp21 were also induced. Conversely, S. mutans proteins in the tricarboxylic acid cycle such as citrate synthase and in the pentose phosphate pathway such as Ribose-5-phosphate isomerase A as well as proteins associated with sugar transport systems were upregulated indicating enhanced carbohydrate metabolism. Interestingly mixed-species biofilm microenvironment had a lower pH than S. mutans single-species biofilms. This observation was supported by proteomics, wherein proteins associated with lactate and formate assimilation such as Glyoxalase and putative NADPH-dependent methylglyoxal reductase proteins were significantly upregulated in the mixed-species biofilms (P<0.05). Furthermore, we unexpectedly found that S. mutans derived glucosyltransferase B (GtfB), responsible for co-adhesion via glucans, can also contribute to C. albicans growth and carbohydrate metabolism by providing glucose and fructose from sucrose breakdown. These findings demonstrate synergistic bacterial-fungal interactions within mixed-species biofilms and a novel GtfB cross-feeding role. Taken together, quantitative proteomics provides new insights into this virulent cross-kingdom oral biofilm.

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Fructose activates a stress response shared by methylglyoxal and hydrogen peroxide in streptococcus mutans

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