Dietary sugars modulate bacterial-fungal interactions in saliva and inter-kingdom biofilm formation on apatitic surface
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , |
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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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) |
repository.mail.fl_str_mv |
|
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1808129325725122560 |