Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study
Dental caries is caused by the formation of cariogenic biofilm, leading to localized areas of enamel demineralization. <i>Streptococcus mutans</i>, a cariogenic pathogen, has long been considered as a microbial etiology of dental caries. We hypothesized that an antagonistic approach usin...
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2022-02-01
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author | Hee-Young Jung Jian-Na Cai Sung Chul Yoo Seon-Hwa Kim Jae-Gyu Jeon Dongyeop Kim |
author_facet | Hee-Young Jung Jian-Na Cai Sung Chul Yoo Seon-Hwa Kim Jae-Gyu Jeon Dongyeop Kim |
author_sort | Hee-Young Jung |
collection | DOAJ |
description | Dental caries is caused by the formation of cariogenic biofilm, leading to localized areas of enamel demineralization. <i>Streptococcus mutans</i>, a cariogenic pathogen, has long been considered as a microbial etiology of dental caries. We hypothesized that an antagonistic approach using a prebiotic collagen peptide in combination with probiotic <i>Lactobacillus rhamnosus</i> would modulate the virulence of this cariogenic biofilm. In vitro <i>S. mutans</i> biofilms were formed on saliva-coated hydroxyapatite discs, and the inhibitory effect of a combination of <i>L. rhamnosus</i> and collagen peptide on <i>S. mutans</i> biofilms were evaluated using microbiological, biochemical, confocal imaging, and transcriptomic analyses. The combination of <i>L. rhamnosus</i> with collagen peptide altered acid production by <i>S. mutans</i>, significantly increasing culture pH at an early stage of biofilm formation. Moreover, the 3D architecture of the <i>S. mutans</i> biofilm was greatly compromised when it was in the presence of <i>L. rhamnosus</i> with collagen peptide, resulting in a significant reduction in exopolysaccharide with unstructured and mixed bacterial organization. The presence of <i>L. rhamnosus</i> with collagen peptide modulated the virulence potential of <i>S. mutans</i> via down-regulation of <i>eno</i>, <i>ldh</i>, and <i>atpD</i> corresponding to acid production and proton transportation, whereas <i>aguD</i> associated with alkali production was up-regulated. Gly-Pro-Hyp, a common tripeptide unit of collagen, consistently modulated the cariogenic potential of <i>S. mutans</i> by inhibiting acid production, similar to the bioactivity of a collagen peptide. It also enhanced the relative abundance of commensal streptococci (<i>S. oralis</i>) in a mixed-species biofilm by inhibiting <i>S. mutans</i> colonization and dome-like microcolony formation. This work demonstrates that food-derived synbiotics may offer a useful means of disrupting cariogenic communities and maintaining microbial homeostasis. |
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spelling | doaj.art-328f865a0b08481a90bdb8e2821edbc82023-11-23T16:47:49ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-02-01233186010.3390/ijms23031860Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro StudyHee-Young Jung0Jian-Na Cai1Sung Chul Yoo2Seon-Hwa Kim3Jae-Gyu Jeon4Dongyeop Kim5Department of Preventive Dentistry, School of Dentistry, Jeonbuk National University, Jeonju 54896, KoreaDepartment of Preventive Dentistry, School of Dentistry, Jeonbuk National University, Jeonju 54896, KoreaVixxol Corporation, Gunpo 15807, KoreaVixxol Corporation, Gunpo 15807, KoreaDepartment of Preventive Dentistry, School of Dentistry, Jeonbuk National University, Jeonju 54896, KoreaDepartment of Preventive Dentistry, School of Dentistry, Jeonbuk National University, Jeonju 54896, KoreaDental caries is caused by the formation of cariogenic biofilm, leading to localized areas of enamel demineralization. <i>Streptococcus mutans</i>, a cariogenic pathogen, has long been considered as a microbial etiology of dental caries. We hypothesized that an antagonistic approach using a prebiotic collagen peptide in combination with probiotic <i>Lactobacillus rhamnosus</i> would modulate the virulence of this cariogenic biofilm. In vitro <i>S. mutans</i> biofilms were formed on saliva-coated hydroxyapatite discs, and the inhibitory effect of a combination of <i>L. rhamnosus</i> and collagen peptide on <i>S. mutans</i> biofilms were evaluated using microbiological, biochemical, confocal imaging, and transcriptomic analyses. The combination of <i>L. rhamnosus</i> with collagen peptide altered acid production by <i>S. mutans</i>, significantly increasing culture pH at an early stage of biofilm formation. Moreover, the 3D architecture of the <i>S. mutans</i> biofilm was greatly compromised when it was in the presence of <i>L. rhamnosus</i> with collagen peptide, resulting in a significant reduction in exopolysaccharide with unstructured and mixed bacterial organization. The presence of <i>L. rhamnosus</i> with collagen peptide modulated the virulence potential of <i>S. mutans</i> via down-regulation of <i>eno</i>, <i>ldh</i>, and <i>atpD</i> corresponding to acid production and proton transportation, whereas <i>aguD</i> associated with alkali production was up-regulated. Gly-Pro-Hyp, a common tripeptide unit of collagen, consistently modulated the cariogenic potential of <i>S. mutans</i> by inhibiting acid production, similar to the bioactivity of a collagen peptide. It also enhanced the relative abundance of commensal streptococci (<i>S. oralis</i>) in a mixed-species biofilm by inhibiting <i>S. mutans</i> colonization and dome-like microcolony formation. This work demonstrates that food-derived synbiotics may offer a useful means of disrupting cariogenic communities and maintaining microbial homeostasis.https://www.mdpi.com/1422-0067/23/3/1860synbioticsprobioticsprebioticscariogenic biofilmsmetabolic interferenceacidogenicity |
spellingShingle | Hee-Young Jung Jian-Na Cai Sung Chul Yoo Seon-Hwa Kim Jae-Gyu Jeon Dongyeop Kim Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study International Journal of Molecular Sciences synbiotics probiotics prebiotics cariogenic biofilms metabolic interference acidogenicity |
title | Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study |
title_full | Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study |
title_fullStr | Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study |
title_full_unstemmed | Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study |
title_short | Collagen Peptide in a Combinatorial Treatment with <i>Lactobacillus rhamnosus</i> Inhibits the Cariogenic Properties of <i>Streptococcus mutans</i>: An In Vitro Study |
title_sort | collagen peptide in a combinatorial treatment with i lactobacillus rhamnosus i inhibits the cariogenic properties of i streptococcus mutans i an in vitro study |
topic | synbiotics probiotics prebiotics cariogenic biofilms metabolic interference acidogenicity |
url | https://www.mdpi.com/1422-0067/23/3/1860 |
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