Antimicrobial effects of commensal oral species are regulated by environmental factors

Herrero, Esteban Rodríguez; Slomka, Vera; Bernaerts, Kristel; Boon, Nico; Hernandez-Sanabria, Emma; Passoni, Bernardo Born; Quirynen, Marc; Teughels, Wim

doi:10.1016/j.jdent.2016.02.007

Cited by 87 publications

(108 citation statements)

References 61 publications

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“…It has been shown that some commensal species can suppress the growth of pathobionts by H 2 O 2 under specific environmental conditions. More specifically, the sequence of colonization and the presence of oxygen are major influencing factors11. Additionally, dysbiotic biofilms are enriched in virulence factors that stimulate the host inflammatory response21.…”

Section: Discussionmentioning

confidence: 99%

“…It has been shown clinically that in patients with periodontal disease, there is a decline in commensal streptococci such as Streptococcus sanguinis 810. It was suggested that H 2 O 2 is one of the most important antimicrobials produced by certain streptococci11. For instance, S. sanguinis and Streptococcus gordonii can inhibit the growth of Streptococcus mutans and Aggregatibacter actinomycetemcomitans by H 2 O 2 production1213.…”

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confidence: 99%

“…For instance, S. sanguinis and Streptococcus gordonii can inhibit the growth of Streptococcus mutans and Aggregatibacter actinomycetemcomitans by H 2 O 2 production1213. Recently, Rodriguez Herrero and coworkers showed that S. oralis , S. gordonii , S. cristatus , S. parasanguinis , S. mitis and S. sanguinis are good H 2 O 2 producers, even under anaerobic conditions11. Although, it has been suggested that H 2 O 2 has an important role in the formation and the composition of the oral biofilms14, the effect of H 2 O 2 production on oral multi-species biofilm composition has not been investigated yet.…”

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Dysbiosis by neutralizing commensal mediated inhibition of pathobionts

Herrero

Slomka

Boon

et al. 2016

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Dysbiosis in the periodontal microbiota is associated with the development of periodontal diseases. Little is known about the initiation of dysbiosis. It was hypothesized that some commensal bacteria suppress the outgrowth of pathobionts by H2O2 production. However, serum and blood components released due to inflammation can neutralize this suppressive effect, leading to the initiation of dysbiosis. Agar plate, dual-species and multi-species ecology experiments showed that H2O2 production by commensal bacteria decreases pathobiont growth and colonization. Peroxidase and blood components neutralize this inhibitory effect primarily by an exogenous peroxidase activity without stimulating growth and biofilm formation of pathobionts directly. In multi-species environments, neutralization of H2O2 resulted in 2 to 3 log increases in pathobionts, a hallmark for dysbiosis. Our data show that in oral biofilms, commensal species suppress the amounts of pathobionts by H2O2 production. Inflammation can neutralize this effect and thereby initiates dysbiosis by allowing the outgrowth of pathobionts.

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Section: Discussionmentioning

confidence: 99%

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Dysbiosis by neutralizing commensal mediated inhibition of pathobionts

Herrero

Slomka

Boon

et al. 2016

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“…A second strategy employed by oral commensal streptococci to achieve a competitive advantage over oral pathogens is the generation of hydrogen peroxide (H 2 O 2 ), which inhibits the growth of S. mutans , the periodontal pathogen Porphyromonas gingivalis (96), and other oral pathogens. Among the known peroxigenic commensals, which include S. oralis , S. mitis , S. sanguinis , S. gordonii and S. oligofermentans , there are multiple enzymatic pathways for the generation of H 2 O 2 .…”

Section: The Good Streptococci: Commensal Oral Floramentioning

confidence: 99%

Biology of Oral Streptococci

et al. 2018

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Summary Bacteria belonging to the genus Streptococcus are the first inhabitants of the oral cavity which can be acquired right after birth and thus play an important role in the assembly of the oral microbiota. In this chapter, we will discuss the different oral environments inhabited by streptococci and the species that occupy each niche. Special attention is given to the taxonomy of Streptococcus as this genus is now divided into 8 distinct groups where oral species are found in 6 of them. Oral streptococci produce an arsenal of adhesive molecules that allow them to efficiently colonize different tissues in the mouth. Also, they have a remarkable ability to metabolize carbohydrates via fermentation thereby generating acids as byproducts. Excessive acidification of the oral environment by aciduric species such as Streptococcus mutans is directly associated with the development of dental caries. However, less acid-tolerant species such as Streptococcus salivarius and Streptococcus gordonii produce large amounts of alkali displaying and important role in the acid-base physiology of the oral cavity. Another important characteristic of certain oral streptococci is their ability to generate hydrogen peroxide that can inhibit the growth of S. mutans. Thus, oral streptococci can also be beneficial to the host by producing molecules that are inhibitory to pathogenic species. Lastly, commensal and pathogenic streptococci residing in the oral cavity can eventually gain access to the bloodstream and cause systemic infections such as infective endocarditis.

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“…13,14–18 The inhibitory effect of H 2 O 2 extends also towards periodontal pathogens such as Aggregatibacter actinomycetemcomitans (Aa). 19 However, the interspecies interaction between Aa and Sg seems to be more intricate since non/lethal concentrations of H 2 O 2 favor survival of Aa against the host innate immunity by inducing a specific transcriptional response 20 tailored towards complement evasion. This indicates that the concentration of H 2 O 2 in the context of a biofilm determines its potential as antimicrobial or signaling component.…”

Section: Introductionmentioning

confidence: 99%

Pt-Decorated MWCNTs–Ionic Liquid Composite-Based Hydrogen Peroxide Sensor To Study Microbial Metabolism Using Scanning Electrochemical Microscopy

2017

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Hydrogen peroxide (H2O2) is a highly relevant metabolite in many biological processes, including the oral microbiome. To study this metabolite, we developed a 25 μm diameter, highly sensitive, non/enzymatic H2O2 sensor with a detection limit of 250 nM and a broad linear range of 250 nM to 7 mM. The sensor used the synergistic activity of the catalytically active Pt nanoparticles on a high surface area multiwall carbon nanotube and conducting ionic liquid matrix to achieve high sensitivity (2.4 ± 0.24 mA cm−2 mM−1) for H2O2 oxidation. The unique composite allowed us to miniaturize the sensor and couple it with a Pt electrode (25 μm diameter each) for use as a dual scanning electrochemical microscopy probe. We could detect 65±10 >M of H2O2 produced by Streptococcus gordonii (Sg) biofilms at a 50 μm above its surface in the presence of 1 mM glucose and artificial saliva solution (pH 7.2 at 37°C). Because of the high stability and low detection limit, the sensor showed a promising chemical image of H2O2 produced by Sg biofilms. We were also able to detect 30 μM of H2O2 at 50 μm above the biofilm in the presence of the H2O2-decomposing salivary lactoperoxidase and thiocyanate, which would not otherwise be possible by existing H2O2 assay. Thus, this sensor can potentially find application in the study of other important biological processes in a complex matrix where circumstance demands a low detection limit in a compact space.

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Antimicrobial effects of commensal oral species are regulated by environmental factors

Cited by 87 publications

References 61 publications

Dysbiosis by neutralizing commensal mediated inhibition of pathobionts

Dysbiosis by neutralizing commensal mediated inhibition of pathobionts

Biology of Oral Streptococci

Pt-Decorated MWCNTs–Ionic Liquid Composite-Based Hydrogen Peroxide Sensor To Study Microbial Metabolism Using Scanning Electrochemical Microscopy

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