The Role of Hydrogen Peroxide in Environmental Adaptation of Oral Microbial Communities

Zhu, Lin; Kreth, Jens

doi:10.1155/2012/717843

Cited by 122 publications

(128 citation statements)

References 81 publications

(127 reference statements)

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“…The production of H 2 O 2 by oral streptococci has been hypothesized to equip the bacteria with the competitive advantage to colonize oral surfaces (22). However, given the bactericidal property of H 2 O 2 , for oral bacteria to successfully coaggregate with oral streptococci in plaque biofilm, bacterial species with mechanisms to overcome the cytotoxic effects of H 2 O 2 should possess a survival advantage in the oral environment (22,23). In addition, during periods of mechanical disruption of dental plaque, anaerobes associated with periodontal disease may be exposed to oxygen.…”

Section: Fig 3 Effects Of H 2 S On Intracellular Sulfide Levels and Gmentioning

confidence: 99%

Reduced Glutathione Mediates Resistance to H ₂ S Toxicity in Oral Streptococci

Ooi

Tan

2016

Appl Environ Microbiol

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Periodontal disease is associated with changes in the composition of the oral microflora, where health-associated oral streptococci decrease while Gram-negative anaerobes predominate in disease. A key feature of periodontal disease-associated anaerobes is their ability to produce hydrogen sulfide (H 2 S) abundantly as a by-product of anaerobic metabolism. So far, H 2 S has been reported to be either cytoprotective or cytotoxic by modulating bacterial antioxidant defense systems. Although oral anaerobes produce large amounts of H 2 S, the potential effects of H 2 S on oral streptococci are currently unknown. The aim of this study was to determine the effects of H 2 S on the survival and biofilm formation of oral streptococci. The growth and biofilm formation of Streptococcus mitis and Streptococcus oralis were inhibited by H 2 S. However, H 2 S did not significantly affect the growth of Streptococcus gordonii or Streptococcus sanguinis. The differential susceptibility of oral streptococci to H 2 S was attributed to differences in the intracellular concentrations of reduced glutathione (GSH). In the absence of GSH, H 2 S elicited its toxicity through an iron-dependent mechanism. Collectively, our results showed that H 2 S exerts antimicrobial effects on certain oral streptococci, potentially contributing to the decrease in health-associated plaque microflora.

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Section: Fig 3 Effects Of H 2 S On Intracellular Sulfide Levels and Gmentioning

confidence: 99%

Reduced Glutathione Mediates Resistance to H ₂ S Toxicity in Oral Streptococci

Ooi

Tan

2016

Appl Environ Microbiol

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“…For all organisms that inhabit the oral cavity, oxidative stresses are relevant threats for which defense mechanisms must be in place. Aside from the presence of hydrogen peroxide (H 2 O 2 ) in oral care products, members of the mitis group of streptococci, which cohabit the dental plaque along with S. mutans, are net producers of H 2 O 2 (3)(4)(5). Notably, there is an inverse correlation between the proportion of S. mutans and of members of the mitis group in health and disease, with high numbers of S. mutans organisms associated with disease and a high proportion of mitis streptococci associated with oral health (6,7).…”

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Transcription of Oxidative Stress Genes Is Directly Activated by SpxA1 and, to a Lesser Extent, by SpxA2 in Streptococcus mutans

et al. 2015

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The SpxA1 and SpxA2 (formerly SpxA and SpxB) transcriptional regulators of Streptococcus mutans are members of a highly conserved family of proteins found in Firmicutes, and they were previously shown to activate oxidative stress responses. In this study, we showed that SpxA1 exerts substantial positive regulatory influence over oxidative stress genes following exposure to H 2 O 2 , while SpxA2 appears to have a secondary regulatory role. In vitro transcription (IVT) assays using purified SpxA1 and/or SpxA2 showed that SpxA1 and, less often, SpxA2 directly activate transcription of some of the major oxidative stress genes. Addition of equimolar concentrations of SpxA1 and SpxA2 to the IVT reactions neither enhanced transcription of the tested genes nor disrupted the dominant role of SpxA1. Substitution of a conserved glycine residue (G52) present in both Spx proteins by arginine (Spx G52R ) resulted in strains that phenocopied the ⌬spx strains. Moreover, addition of purified SpxA1 G52R completely failed to activate transcription of ahpC, sodA, and tpx, further confirming that the G52 residue is critical for Spx functionality. IMPORTANCEStreptococcus mutans is a pathogen associated with the formation of dental caries in humans. Within the oral cavity, S. mutans routinely encounters oxidative stress. Our previous data revealed that two regulatory proteins, SpxA1 and SpxA2 (formerly SpxA and SpxB), bear high homology to the Spx regulator that has been characterized as a critical activator of oxidative stress genes in Bacillus subtilis. In this report, we prove that Spx proteins of S. mutans directly activate transcription of genes involved in the oxidative stress response, though SpxA1 appears to have a more dominant role than SpxA2. Therefore, the Spx regulators play a critical role in the ability of S. mutans to thrive within the oral cavity.T he oral cavity is colonized by hundreds of bacterial species, some of which contribute to overall oral health and others that are associated with disease, such as dental caries and periodontitis. Among the pathogenic oral bacteria, clinical evidence paired with in vitro and in vivo studies strongly associates Streptococcus mutans with dental caries onset and development (1, 2). For all organisms that inhabit the oral cavity, oxidative stresses are relevant threats for which defense mechanisms must be in place. Aside from the presence of hydrogen peroxide (H 2 O 2 ) in oral care products, members of the mitis group of streptococci, which cohabit the dental plaque along with S. mutans, are net producers of H 2 O 2 (3-5). Notably, there is an inverse correlation between the proportion of S. mutans and of members of the mitis group in health and disease, with high numbers of S. mutans organisms associated with disease and a high proportion of mitis streptococci associated with oral health (6, 7). Ultimately, the breakdown of H 2 O 2 into other variants of reactive oxygen species (ROS) can disturb the integrity of DNA and proteins and thereby pose a significant threat to...

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“…S. oralis is frequently isolated from cases of infective endocarditis (7-10), and ribosomal DNAs of the mitis group were detected in atheromatous plaque (11). The rate of bacteremia caused by members of the mitis group of streptococci is comparable to that caused by group A or B streptococci (12).The members of the mitis group of streptococci produce hydrogen peroxide (H 2 O 2 ) (2, 13, 14), which is important in bacterial competition in microbial communities, such as oral biofilms (13,14). S. sanguinis and S. gordonii produce H 2 O 2 in quantities sufficient to reduce the growth of many oral bacteria, including the cariogenic bacterium Streptococcus mutans and several periodontal pathogens (13,14).…”

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confidence: 99%

“…The members of the mitis group of streptococci produce hydrogen peroxide (H 2 O 2 ) (2, 13, 14), which is important in bacterial competition in microbial communities, such as oral biofilms (13,14). S. sanguinis and S. gordonii produce H 2 O 2 in quantities sufficient to reduce the growth of many oral bacteria, including the cariogenic bacterium Streptococcus mutans and several periodontal pathogens (13,14).…”

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Streptococcus oralis Induces Lysosomal Impairment of Macrophages via Bacterial Hydrogen Peroxide

et al. 2016

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c Streptococcus oralis, an oral commensal, belongs to the mitis group of streptococci and occasionally causes opportunistic infections, such as bacterial endocarditis and bacteremia. Recently, we found that the hydrogen peroxide (H 2 O 2 ) produced by S. oralis is sufficient to kill human monocytes and epithelial cells, implying that streptococcal H 2 O 2 is a cytotoxin. In the present study, we investigated whether streptococcal H 2 O 2 impacts lysosomes, organelles of the intracellular digestive system, in relation to cell death. S. oralis infection induced the death of RAW 264 macrophages in an H 2 O 2 -dependent manner, which was exemplified by the fact that exogenous H 2 O 2 also induced cell death. Infection with either a mutant lacking spxB, which encodes pyruvate oxidase responsible for H 2 O 2 production, or Streptococcus mutans, which does not produce H 2 O 2 , showed less cytotoxicity. Visualization of lysosomes with LysoTracker revealed lysosome deacidification after infection with S. oralis or exposure to H 2 O 2 , which was corroborated by acridine orange staining. Similarly, fluorescent labeling of lysosome-associated membrane protein-1 gradually disappeared during infection with S. oralis or exposure to H 2 O 2 . The deacidification and the following induction of cell death were inhibited by chelating iron in lysosomes. Moreover, fluorescent staining of cathepsin B indicated lysosomal destruction. However, treatment of infected cells with a specific inhibitor of cathepsin B had negligible effects on cell death; instead, it suppressed the detachment of dead cells from the culture plates. These results suggest that streptococcal H 2 O 2 induces cell death with lysosomal destruction and then the released lysosomal cathepsins contribute to the detachment of the dead cells. Streptococcus oralis, a commensal bacterium in the oral cavity, belongs to the group of oral inhabitants of the mitis group of streptococci (1-4). Members of this group, including Streptococcus sanguinis and Streptococcus gordonii, are dominant colonizers of human teeth and are involved in dental plaque formation (1-3). Pathogenic streptococcal species, such as Streptococcus pneumoniae and Streptococcus mitis, are also members of the mitis group (2, 4-6). This group has been implicated as a possible cause of human cardiovascular diseases, including infective endocarditis and atherosclerosis. S. oralis is frequently isolated from cases of infective endocarditis (7-10), and ribosomal DNAs of the mitis group were detected in atheromatous plaque (11). The rate of bacteremia caused by members of the mitis group of streptococci is comparable to that caused by group A or B streptococci (12).The members of the mitis group of streptococci produce hydrogen peroxide (H 2 O 2 ) (2, 13, 14), which is important in bacterial competition in microbial communities, such as oral biofilms (13,14). S. sanguinis and S. gordonii produce H 2 O 2 in quantities sufficient to reduce the growth of many oral bacteria, including the cariogenic bacterium Strepto...

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The Role of Hydrogen Peroxide in Environmental Adaptation of Oral Microbial Communities

Cited by 122 publications

References 81 publications

Reduced Glutathione Mediates Resistance to H ₂ S Toxicity in Oral Streptococci

Reduced Glutathione Mediates Resistance to H ₂ S Toxicity in Oral Streptococci

Transcription of Oxidative Stress Genes Is Directly Activated by SpxA1 and, to a Lesser Extent, by SpxA2 in Streptococcus mutans

Streptococcus oralis Induces Lysosomal Impairment of Macrophages via Bacterial Hydrogen Peroxide

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The Role of Hydrogen Peroxide in Environmental Adaptation of Oral Microbial Communities

Cited by 122 publications

References 81 publications

Reduced Glutathione Mediates Resistance to H 2 S Toxicity in Oral Streptococci

Reduced Glutathione Mediates Resistance to H 2 S Toxicity in Oral Streptococci

Transcription of Oxidative Stress Genes Is Directly Activated by SpxA1 and, to a Lesser Extent, by SpxA2 in Streptococcus mutans

Streptococcus oralis Induces Lysosomal Impairment of Macrophages via Bacterial Hydrogen Peroxide

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Reduced Glutathione Mediates Resistance to H ₂ S Toxicity in Oral Streptococci

Reduced Glutathione Mediates Resistance to H ₂ S Toxicity in Oral Streptococci