Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries

Detalhes bibliográficos
Autor(a) principal: Kim, Dongyeop
Data de Publicação: 2020
Outros Autores: Barraza, Juan P., Arthur, Rodrigo Alex, Hara, Anderson Takeo, Lewis, Karl J., Liu, Yuan, Scisci, Elizabeth L., Hajishengallis, Evlambia, Whiteley, Marvin, Koo, Hyun
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFRGS
Texto Completo: http://hdl.handle.net/10183/239945
Resumo: Tooth decay (dental caries) is a widespread human disease caused by microbial biofilms. Streptococcus mutans, a biofilm-former, has been consistently associated with severe childhood caries; however, how this bacterium is spatially organized with other microorganisms in the oral cavity to promote disease remains unknown. Using intact biofilms formed on teeth of toddlers affected by caries, we discovered a unique 3D rotund-shaped architecture composed of multiple species precisely arranged in a corona-like structure with an inner core of S. mutans encompassed by outer layers of other bacteria. This architecture creates localized regions of acidic pH and acute enamel demineralization (caries) in a mixed-species biofilm model on human teeth, suggesting this highly ordered community as the causative agent. Notably, the construction of this architecture was found to be an active process initiated by production of an extracellular scaffold by S. mutans that assembles the corona cell arrangement, encapsulating the pathogen core. In addition, this spatial patterning creates a protective barrier against antimicrobials while increasing bacterial acid fitness associated with the disease-causing state. Our data reveal a precise biogeography in a polymicrobial community associated with human caries that can modulate the pathogen positioning and virulence potential in situ, indicating that micron-scale spatial structure of the microbiome may mediate the function and outcome of host-pathogen interactions.
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spelling Kim, DongyeopBarraza, Juan P.Arthur, Rodrigo AlexHara, Anderson TakeoLewis, Karl J.Liu, YuanScisci, Elizabeth L.Hajishengallis, EvlambiaWhiteley, MarvinKoo, Hyun2022-06-07T04:41:48Z20200027-8424http://hdl.handle.net/10183/239945001137985Tooth decay (dental caries) is a widespread human disease caused by microbial biofilms. Streptococcus mutans, a biofilm-former, has been consistently associated with severe childhood caries; however, how this bacterium is spatially organized with other microorganisms in the oral cavity to promote disease remains unknown. Using intact biofilms formed on teeth of toddlers affected by caries, we discovered a unique 3D rotund-shaped architecture composed of multiple species precisely arranged in a corona-like structure with an inner core of S. mutans encompassed by outer layers of other bacteria. This architecture creates localized regions of acidic pH and acute enamel demineralization (caries) in a mixed-species biofilm model on human teeth, suggesting this highly ordered community as the causative agent. Notably, the construction of this architecture was found to be an active process initiated by production of an extracellular scaffold by S. mutans that assembles the corona cell arrangement, encapsulating the pathogen core. In addition, this spatial patterning creates a protective barrier against antimicrobials while increasing bacterial acid fitness associated with the disease-causing state. Our data reveal a precise biogeography in a polymicrobial community associated with human caries that can modulate the pathogen positioning and virulence potential in situ, indicating that micron-scale spatial structure of the microbiome may mediate the function and outcome of host-pathogen interactions.application/pdfengProceedings of the national academy of sciences of the united states of america. Washington. Vol. 117, no. 22 (June 2020), p. 12375–12386Cárie dentáriaMicrobiotaBiogeografiaBiofilmesStreptococcus mutansDental cariesPolymicrobialBiogeographyBiofilmStreptococcus mutansSpatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental cariesEstrangeiroinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFRGSinstname:Universidade Federal do Rio Grande do Sul (UFRGS)instacron:UFRGSTEXT001137985.pdf.txt001137985.pdf.txtExtracted Texttext/plain69822http://www.lume.ufrgs.br/bitstream/10183/239945/2/001137985.pdf.txtb842999bdffa8d1c43cd01bfe68ba4e1MD52ORIGINAL001137985.pdfTexto completo (inglês)application/pdf3698800http://www.lume.ufrgs.br/bitstream/10183/239945/1/001137985.pdfbca083b8400bc7130a15eba9d5ae05feMD5110183/2399452022-06-08 04:41:20.842111oai:www.lume.ufrgs.br:10183/239945Repositório de PublicaçõesPUBhttps://lume.ufrgs.br/oai/requestopendoar:2022-06-08T07:41:20Repositório Institucional da UFRGS - Universidade Federal do Rio Grande do Sul (UFRGS)false
dc.title.pt_BR.fl_str_mv Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
title Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
spellingShingle Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
Kim, Dongyeop
Cárie dentária
Microbiota
Biogeografia
Biofilmes
Streptococcus mutans
Dental caries
Polymicrobial
Biogeography
Biofilm
Streptococcus mutans
title_short Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
title_full Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
title_fullStr Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
title_full_unstemmed Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
title_sort Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries
author Kim, Dongyeop
author_facet Kim, Dongyeop
Barraza, Juan P.
Arthur, Rodrigo Alex
Hara, Anderson Takeo
Lewis, Karl J.
Liu, Yuan
Scisci, Elizabeth L.
Hajishengallis, Evlambia
Whiteley, Marvin
Koo, Hyun
author_role author
author2 Barraza, Juan P.
Arthur, Rodrigo Alex
Hara, Anderson Takeo
Lewis, Karl J.
Liu, Yuan
Scisci, Elizabeth L.
Hajishengallis, Evlambia
Whiteley, Marvin
Koo, Hyun
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Kim, Dongyeop
Barraza, Juan P.
Arthur, Rodrigo Alex
Hara, Anderson Takeo
Lewis, Karl J.
Liu, Yuan
Scisci, Elizabeth L.
Hajishengallis, Evlambia
Whiteley, Marvin
Koo, Hyun
dc.subject.por.fl_str_mv Cárie dentária
Microbiota
Biogeografia
Biofilmes
Streptococcus mutans
topic Cárie dentária
Microbiota
Biogeografia
Biofilmes
Streptococcus mutans
Dental caries
Polymicrobial
Biogeography
Biofilm
Streptococcus mutans
dc.subject.eng.fl_str_mv Dental caries
Polymicrobial
Biogeography
Biofilm
Streptococcus mutans
description Tooth decay (dental caries) is a widespread human disease caused by microbial biofilms. Streptococcus mutans, a biofilm-former, has been consistently associated with severe childhood caries; however, how this bacterium is spatially organized with other microorganisms in the oral cavity to promote disease remains unknown. Using intact biofilms formed on teeth of toddlers affected by caries, we discovered a unique 3D rotund-shaped architecture composed of multiple species precisely arranged in a corona-like structure with an inner core of S. mutans encompassed by outer layers of other bacteria. This architecture creates localized regions of acidic pH and acute enamel demineralization (caries) in a mixed-species biofilm model on human teeth, suggesting this highly ordered community as the causative agent. Notably, the construction of this architecture was found to be an active process initiated by production of an extracellular scaffold by S. mutans that assembles the corona cell arrangement, encapsulating the pathogen core. In addition, this spatial patterning creates a protective barrier against antimicrobials while increasing bacterial acid fitness associated with the disease-causing state. Our data reveal a precise biogeography in a polymicrobial community associated with human caries that can modulate the pathogen positioning and virulence potential in situ, indicating that micron-scale spatial structure of the microbiome may mediate the function and outcome of host-pathogen interactions.
publishDate 2020
dc.date.issued.fl_str_mv 2020
dc.date.accessioned.fl_str_mv 2022-06-07T04:41:48Z
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dc.relation.ispartof.pt_BR.fl_str_mv Proceedings of the national academy of sciences of the united states of america. Washington. Vol. 117, no. 22 (June 2020), p. 12375–12386
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