Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study

Early childhood caries, a virulent-form of dental caries, is painful, difficult, and costly to treat that has been associated with high levels of Streptococcus mutans (Sm) and Candida albicans (Ca) in plaque-biofilms on teeth. These microorganisms appear to develop a symbiotic cross-kingdom interact...

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Main Authors: Hye-Eun Kim, Yuan Liu, Atul Dhall, Marwa Bawazir, Hyun Koo, Geelsu Hwang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-02-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2020.623980/full
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spelling doaj-9be449ae236b4106a74b0843754990cc2021-02-19T07:12:59ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882021-02-011010.3389/fcimb.2020.623980623980Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro StudyHye-Eun Kim0Yuan Liu1Atul Dhall2Marwa Bawazir3Hyun Koo4Hyun Koo5Geelsu Hwang6Geelsu Hwang7Department of Preventive and Restorative Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Preventive and Restorative Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Preventive and Restorative Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Preventive and Restorative Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Orthodontics, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, United StatesCenter for Innovation & Precision Dentistry, School of Dental Medicine, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, PA, United StatesDepartment of Preventive and Restorative Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, PA, United StatesCenter for Innovation & Precision Dentistry, School of Dental Medicine, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, PA, United StatesEarly childhood caries, a virulent-form of dental caries, is painful, difficult, and costly to treat that has been associated with high levels of Streptococcus mutans (Sm) and Candida albicans (Ca) in plaque-biofilms on teeth. These microorganisms appear to develop a symbiotic cross-kingdom interaction that amplifies the virulence of plaque-biofilms. Although biofilm studies reveal synergistic bacterial-fungal association, how these organisms modulate cross-kingdom biofilm formation and enhance its virulence in the presence of saliva remain largely unknown. Here, we compared the properties of Sm and Sm-Ca biofilms cultured in saliva by examining the biofilm structural organization and capability to sustain an acidic pH environment conducive to enamel demineralization. Intriguingly, Sm-Ca biofilm is rapidly matured and maintained acidic pH-values (~4.3), while Sm biofilm development was retarded and failed to create an acidic environment when cultured in saliva. In turn, the human enamel slab surface was severely demineralized by Sm-Ca biofilms, while there was minimal damage to the enamel surface by Sm biofilm. Interestingly, Sm-Ca biofilms exhibited an acidic environment regardless of their hyphal formation ability. Our data reveal the critical role of symbiotic interaction between S. mutans and C. albicans in human saliva in the context of pathogenesis of dental caries, which may explain how the cross-kingdom interaction contributes to enhanced virulence of plaque-biofilm in the oral cavity.https://www.frontiersin.org/articles/10.3389/fcimb.2020.623980/fullcross-kingdom biofilmStreptococcus mutansCandida albicanshuman salivaacidogenicityenamel demineralization
collection DOAJ
language English
format Article
sources DOAJ
author Hye-Eun Kim
Yuan Liu
Atul Dhall
Marwa Bawazir
Hyun Koo
Hyun Koo
Geelsu Hwang
Geelsu Hwang
spellingShingle Hye-Eun Kim
Yuan Liu
Atul Dhall
Marwa Bawazir
Hyun Koo
Hyun Koo
Geelsu Hwang
Geelsu Hwang
Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study
Frontiers in Cellular and Infection Microbiology
cross-kingdom biofilm
Streptococcus mutans
Candida albicans
human saliva
acidogenicity
enamel demineralization
author_facet Hye-Eun Kim
Yuan Liu
Atul Dhall
Marwa Bawazir
Hyun Koo
Hyun Koo
Geelsu Hwang
Geelsu Hwang
author_sort Hye-Eun Kim
title Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study
title_short Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study
title_full Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study
title_fullStr Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study
title_full_unstemmed Synergism of Streptococcus mutans and Candida albicans Reinforces Biofilm Maturation and Acidogenicity in Saliva: An In Vitro Study
title_sort synergism of streptococcus mutans and candida albicans reinforces biofilm maturation and acidogenicity in saliva: an in vitro study
publisher Frontiers Media S.A.
series Frontiers in Cellular and Infection Microbiology
issn 2235-2988
publishDate 2021-02-01
description Early childhood caries, a virulent-form of dental caries, is painful, difficult, and costly to treat that has been associated with high levels of Streptococcus mutans (Sm) and Candida albicans (Ca) in plaque-biofilms on teeth. These microorganisms appear to develop a symbiotic cross-kingdom interaction that amplifies the virulence of plaque-biofilms. Although biofilm studies reveal synergistic bacterial-fungal association, how these organisms modulate cross-kingdom biofilm formation and enhance its virulence in the presence of saliva remain largely unknown. Here, we compared the properties of Sm and Sm-Ca biofilms cultured in saliva by examining the biofilm structural organization and capability to sustain an acidic pH environment conducive to enamel demineralization. Intriguingly, Sm-Ca biofilm is rapidly matured and maintained acidic pH-values (~4.3), while Sm biofilm development was retarded and failed to create an acidic environment when cultured in saliva. In turn, the human enamel slab surface was severely demineralized by Sm-Ca biofilms, while there was minimal damage to the enamel surface by Sm biofilm. Interestingly, Sm-Ca biofilms exhibited an acidic environment regardless of their hyphal formation ability. Our data reveal the critical role of symbiotic interaction between S. mutans and C. albicans in human saliva in the context of pathogenesis of dental caries, which may explain how the cross-kingdom interaction contributes to enhanced virulence of plaque-biofilm in the oral cavity.
topic cross-kingdom biofilm
Streptococcus mutans
Candida albicans
human saliva
acidogenicity
enamel demineralization
url https://www.frontiersin.org/articles/10.3389/fcimb.2020.623980/full
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