The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging.
The formation of multicellular communities known as biofilms is the part of bacterial life cycle in which bacteria display cooperative behaviour and differentiated phenotypes leading to specific functions. Bacillus subtilis is a Gram-positive bacterium that has served for a decade as a model to stud...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2011-01-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC3022735?pdf=render |
| _version_ | 1818290849923989504 |
|---|---|
| author | Arnaud Bridier Arnaud Bridier Dominique Le Coq Florence Dubois-Brissonnet Vincent Thomas Stéphane Aymerich Romain Briandet |
| author_facet | Arnaud Bridier Arnaud Bridier Dominique Le Coq Florence Dubois-Brissonnet Vincent Thomas Stéphane Aymerich Romain Briandet |
| author_sort | Arnaud Bridier |
| collection | DOAJ |
| description | The formation of multicellular communities known as biofilms is the part of bacterial life cycle in which bacteria display cooperative behaviour and differentiated phenotypes leading to specific functions. Bacillus subtilis is a Gram-positive bacterium that has served for a decade as a model to study the molecular pathways that control biofilm formation. Most of the data on B. subtilis biofilms have come from studies on the formation of pellicles at the air-liquid interface, or on the complex macrocolonies that develop on semi-solid nutritive agar. Here, using confocal laser scanning microcopy, we show that B. subtilis strains of different origins are capable of forming biofilms on immersed surfaces with dramatically protruding "beanstalk-like" structures with certain strains. Indeed, these structures can reach a height of more than 300 µm with one undomesticated strain from a medical environment. Using 14 GFP-labeled mutants previously described as affecting pellicle or complex colony formation, we have identified four genes whose inactivation significantly impeded immersed biofilm development, and one mutation triggering hyperbiofilm formation. We also identified mutations causing the three-dimensional architecture of the biofilm to be altered. Taken together, our results reveal that B. subtilis is able to form specific biofilm features on immersed surfaces, and that the development of these multicellular surface-associated communities involves regulation pathways that are common to those governing the formation of pellicle and/or complex colonies, and also some specific mechanisms. Finally, we propose the submerged surface-associated biofilm as another relevant model for the study of B. subtilis multicellular communities. |
| first_indexed | 2024-12-13T02:34:43Z |
| format | Article |
| id | doaj.art-28693d914a3d489db6a18a375724015d |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-13T02:34:43Z |
| publishDate | 2011-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-28693d914a3d489db6a18a375724015d2022-12-22T00:02:25ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0161e1617710.1371/journal.pone.0016177The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging.Arnaud BridierArnaud BridierDominique Le CoqFlorence Dubois-BrissonnetVincent ThomasStéphane AymerichRomain BriandetThe formation of multicellular communities known as biofilms is the part of bacterial life cycle in which bacteria display cooperative behaviour and differentiated phenotypes leading to specific functions. Bacillus subtilis is a Gram-positive bacterium that has served for a decade as a model to study the molecular pathways that control biofilm formation. Most of the data on B. subtilis biofilms have come from studies on the formation of pellicles at the air-liquid interface, or on the complex macrocolonies that develop on semi-solid nutritive agar. Here, using confocal laser scanning microcopy, we show that B. subtilis strains of different origins are capable of forming biofilms on immersed surfaces with dramatically protruding "beanstalk-like" structures with certain strains. Indeed, these structures can reach a height of more than 300 µm with one undomesticated strain from a medical environment. Using 14 GFP-labeled mutants previously described as affecting pellicle or complex colony formation, we have identified four genes whose inactivation significantly impeded immersed biofilm development, and one mutation triggering hyperbiofilm formation. We also identified mutations causing the three-dimensional architecture of the biofilm to be altered. Taken together, our results reveal that B. subtilis is able to form specific biofilm features on immersed surfaces, and that the development of these multicellular surface-associated communities involves regulation pathways that are common to those governing the formation of pellicle and/or complex colonies, and also some specific mechanisms. Finally, we propose the submerged surface-associated biofilm as another relevant model for the study of B. subtilis multicellular communities.http://europepmc.org/articles/PMC3022735?pdf=render |
| spellingShingle | Arnaud Bridier Arnaud Bridier Dominique Le Coq Florence Dubois-Brissonnet Vincent Thomas Stéphane Aymerich Romain Briandet The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging. PLoS ONE |
| title | The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging. |
| title_full | The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging. |
| title_fullStr | The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging. |
| title_full_unstemmed | The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging. |
| title_short | The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in situ imaging. |
| title_sort | spatial architecture of bacillus subtilis biofilms deciphered using a surface associated model and in situ imaging |
| url | http://europepmc.org/articles/PMC3022735?pdf=render |
| work_keys_str_mv | AT arnaudbridier thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT arnaudbridier thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT dominiquelecoq thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT florenceduboisbrissonnet thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT vincentthomas thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT stephaneaymerich thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT romainbriandet thespatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT arnaudbridier spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT arnaudbridier spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT dominiquelecoq spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT florenceduboisbrissonnet spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT vincentthomas spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT stephaneaymerich spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging AT romainbriandet spatialarchitectureofbacillussubtilisbiofilmsdecipheredusingasurfaceassociatedmodelandinsituimaging |