Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface

Detalhes bibliográficos
Autor(a) principal: Negrini, Thais de Cássia [UNESP]
Data de Publicação: 2022
Outros Autores: Ren, Zhi, Miao, Yilan, Kim, Dongyeop, Simon-Soro, Áurea, Liu, Yuan, Koo, Hyun, Arthur, Rodrigo Alex
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.3389/fcimb.2022.993640
http://hdl.handle.net/11449/247931
Resumo: Bacteria and fungi can interact to form inter-kingdom biofilms in the oral cavity. Streptococcus mutans and Candida albicans are frequently detected in saliva and in dental biofilms associated with early childhood caries (tooth-decay), a prevalent oral disease induced by dietary sugars. However, how different sugars influence this bacterial-fungal interaction remains unclear. Here, we investigate whether specific sugars affect the inter-kingdom interaction in saliva and subsequent biofilm formation on tooth-mimetic surfaces. The microbes were incubated in saliva containing common dietary sugars (glucose and fructose, sucrose, starch, and combinations) and analyzed via fluorescence imaging and quantitative computational analyses. The bacterial and fungal cells in saliva were then transferred to hydroxyapatite discs (tooth mimic) to allow microbial binding and biofilm development. We found diverse bacterial-fungal aggregates which varied in size, structure, and spatial organization depending on the type of sugars. Sucrose and starch+sucrose induced the formation of large mixed-species aggregates characterized by bacterial clusters co-bound with fungal cells, whereas mostly single-cells were found in the absence of sugar or in the presence of glucose and fructose. Notably, both colonization and further growth on the apatitic surface were dependent on sugar-mediated aggregation, leading to biofilms with distinctive spatial organizations and 3D architectures. Starch+sucrose and sucrose-mediated aggregates developed into large and highly acidogenic biofilms with complex network of bacterial and fungal cells (yeast and hyphae) surrounded by an intricate matrix of extracellular glucans. In contrast, biofilms originated from glucose and fructose-mediated consortia (or without sugar) were sparsely distributed on the surface without structural integration, growing predominantly as individual species with reduced acidogenicity. These findings reveal the impact of dietary sugars on inter-kingdom interactions in saliva and how they mediate biofilm formation with distinctive structural organization and varying acidogenicity implicated with human tooth-decay.
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spelling Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surfaceC. albicansEPSinter-kingdom aggregateS. mutanssalivasucroseBacteria and fungi can interact to form inter-kingdom biofilms in the oral cavity. Streptococcus mutans and Candida albicans are frequently detected in saliva and in dental biofilms associated with early childhood caries (tooth-decay), a prevalent oral disease induced by dietary sugars. However, how different sugars influence this bacterial-fungal interaction remains unclear. Here, we investigate whether specific sugars affect the inter-kingdom interaction in saliva and subsequent biofilm formation on tooth-mimetic surfaces. The microbes were incubated in saliva containing common dietary sugars (glucose and fructose, sucrose, starch, and combinations) and analyzed via fluorescence imaging and quantitative computational analyses. The bacterial and fungal cells in saliva were then transferred to hydroxyapatite discs (tooth mimic) to allow microbial binding and biofilm development. We found diverse bacterial-fungal aggregates which varied in size, structure, and spatial organization depending on the type of sugars. Sucrose and starch+sucrose induced the formation of large mixed-species aggregates characterized by bacterial clusters co-bound with fungal cells, whereas mostly single-cells were found in the absence of sugar or in the presence of glucose and fructose. Notably, both colonization and further growth on the apatitic surface were dependent on sugar-mediated aggregation, leading to biofilms with distinctive spatial organizations and 3D architectures. Starch+sucrose and sucrose-mediated aggregates developed into large and highly acidogenic biofilms with complex network of bacterial and fungal cells (yeast and hyphae) surrounded by an intricate matrix of extracellular glucans. In contrast, biofilms originated from glucose and fructose-mediated consortia (or without sugar) were sparsely distributed on the surface without structural integration, growing predominantly as individual species with reduced acidogenicity. These findings reveal the impact of dietary sugars on inter-kingdom interactions in saliva and how they mediate biofilm formation with distinctive structural organization and varying acidogenicity implicated with human tooth-decay.Biofilm Research Laboratories Center for Innovation & Precision Dentistry School of Dental Medicine University of PennsylvaniaDepartment of Orthodontics and Divisions of Pediatric Dentistry & Community Oral Health School of Dental Medicine University of PennsylvaniaDepartment of Clinical Analysis School of Pharmaceutical Sciences Sao Paulo State UniversityDepartment of Preventive Dentistry School of Dentistry Institute of Oral Bioscience Jeonbuk National UniversityDepartment of Stomatology School of Dentistry University of SevillePreventive & Restorative Sciences School of Dental Medicine University of PennsylvaniaDepartment of Preventive and Community Dentistry Dental School Federal University of Rio Grande do SulDepartment of Clinical Analysis School of Pharmaceutical Sciences Sao Paulo State UniversityUniversity of PennsylvaniaUniversidade Estadual Paulista (UNESP)Jeonbuk National UniversityUniversity of SevilleFederal University of Rio Grande do SulNegrini, Thais de Cássia [UNESP]Ren, ZhiMiao, YilanKim, DongyeopSimon-Soro, ÁureaLiu, YuanKoo, HyunArthur, Rodrigo Alex2023-07-29T13:29:50Z2023-07-29T13:29:50Z2022-11-09info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.3389/fcimb.2022.993640Frontiers in Cellular and Infection Microbiology, v. 12.2235-2988http://hdl.handle.net/11449/24793110.3389/fcimb.2022.9936402-s2.0-85142424405Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengFrontiers in Cellular and Infection Microbiologyinfo:eu-repo/semantics/openAccess2024-06-21T15:19:21Zoai:repositorio.unesp.br:11449/247931Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T21:29:30.439167Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
title Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
spellingShingle Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
Negrini, Thais de Cássia [UNESP]
C. albicans
EPS
inter-kingdom aggregate
S. mutans
saliva
sucrose
title_short Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
title_full Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
title_fullStr Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
title_full_unstemmed Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
title_sort Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
author Negrini, Thais de Cássia [UNESP]
author_facet Negrini, Thais de Cássia [UNESP]
Ren, Zhi
Miao, Yilan
Kim, Dongyeop
Simon-Soro, Áurea
Liu, Yuan
Koo, Hyun
Arthur, Rodrigo Alex
author_role author
author2 Ren, Zhi
Miao, Yilan
Kim, Dongyeop
Simon-Soro, Áurea
Liu, Yuan
Koo, Hyun
Arthur, Rodrigo Alex
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv University of Pennsylvania
Universidade Estadual Paulista (UNESP)
Jeonbuk National University
University of Seville
Federal University of Rio Grande do Sul
dc.contributor.author.fl_str_mv Negrini, Thais de Cássia [UNESP]
Ren, Zhi
Miao, Yilan
Kim, Dongyeop
Simon-Soro, Áurea
Liu, Yuan
Koo, Hyun
Arthur, Rodrigo Alex
dc.subject.por.fl_str_mv C. albicans
EPS
inter-kingdom aggregate
S. mutans
saliva
sucrose
topic C. albicans
EPS
inter-kingdom aggregate
S. mutans
saliva
sucrose
description Bacteria and fungi can interact to form inter-kingdom biofilms in the oral cavity. Streptococcus mutans and Candida albicans are frequently detected in saliva and in dental biofilms associated with early childhood caries (tooth-decay), a prevalent oral disease induced by dietary sugars. However, how different sugars influence this bacterial-fungal interaction remains unclear. Here, we investigate whether specific sugars affect the inter-kingdom interaction in saliva and subsequent biofilm formation on tooth-mimetic surfaces. The microbes were incubated in saliva containing common dietary sugars (glucose and fructose, sucrose, starch, and combinations) and analyzed via fluorescence imaging and quantitative computational analyses. The bacterial and fungal cells in saliva were then transferred to hydroxyapatite discs (tooth mimic) to allow microbial binding and biofilm development. We found diverse bacterial-fungal aggregates which varied in size, structure, and spatial organization depending on the type of sugars. Sucrose and starch+sucrose induced the formation of large mixed-species aggregates characterized by bacterial clusters co-bound with fungal cells, whereas mostly single-cells were found in the absence of sugar or in the presence of glucose and fructose. Notably, both colonization and further growth on the apatitic surface were dependent on sugar-mediated aggregation, leading to biofilms with distinctive spatial organizations and 3D architectures. Starch+sucrose and sucrose-mediated aggregates developed into large and highly acidogenic biofilms with complex network of bacterial and fungal cells (yeast and hyphae) surrounded by an intricate matrix of extracellular glucans. In contrast, biofilms originated from glucose and fructose-mediated consortia (or without sugar) were sparsely distributed on the surface without structural integration, growing predominantly as individual species with reduced acidogenicity. These findings reveal the impact of dietary sugars on inter-kingdom interactions in saliva and how they mediate biofilm formation with distinctive structural organization and varying acidogenicity implicated with human tooth-decay.
publishDate 2022
dc.date.none.fl_str_mv 2022-11-09
2023-07-29T13:29:50Z
2023-07-29T13:29:50Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.3389/fcimb.2022.993640
Frontiers in Cellular and Infection Microbiology, v. 12.
2235-2988
http://hdl.handle.net/11449/247931
10.3389/fcimb.2022.993640
2-s2.0-85142424405
url http://dx.doi.org/10.3389/fcimb.2022.993640
http://hdl.handle.net/11449/247931
identifier_str_mv Frontiers in Cellular and Infection Microbiology, v. 12.
2235-2988
10.3389/fcimb.2022.993640
2-s2.0-85142424405
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Frontiers in Cellular and Infection Microbiology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
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