Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members
In nature, bacteria frequently reside in differentiated communities or biofilms. These multicellular communities are held together by self-produced polymers that allow the community members to adhere to the surface as well as to neighbor bacteria. Here, we report that exopolysaccharides prevent Baci...
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| Format: | Article |
| Language: | English |
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Elsevier
2022-01-01
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| Series: | Computational and Structural Biotechnology Journal |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2001037021005080 |
| _version_ | 1797978291908378624 |
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| author | Harsh Maan Tatyana L. Povolotsky Ziv Porat Maxim Itkin Sergey Malitsky Ilana Kolodkin-Gal |
| author_facet | Harsh Maan Tatyana L. Povolotsky Ziv Porat Maxim Itkin Sergey Malitsky Ilana Kolodkin-Gal |
| author_sort | Harsh Maan |
| collection | DOAJ |
| description | In nature, bacteria frequently reside in differentiated communities or biofilms. These multicellular communities are held together by self-produced polymers that allow the community members to adhere to the surface as well as to neighbor bacteria. Here, we report that exopolysaccharides prevent Bacillus subtilis from co-aggregating with a distantly related bacterium Bacillus mycoides, while maintaining their role in promoting self-adhesion and co-adhesion with phylogenetically related bacterium, Bacillus atrophaeus. The defensive role of the exopolysaccharides is due to the specific regulation of bacillaene. Single cell analysis of biofilm and free-living bacterial cells using imaging flow cytometry confirmed a specific role for the exopolysaccharides in microbial competition repelling B. mycoides. Unlike exopolysaccharides, the matrix protein TasA induced bacillaene but inhibited the expression of the biosynthetic clusters for surfactin, and therefore its overall effect on microbial competition during floating biofilm formation was neutral. Thus, the exopolysaccharides provide a dual fitness advantage for biofilm-forming cells, as it acts to promote co-aggregation of related species, as well as, a secreted cue for chemical interference with non-compatible partners. These results experimentally demonstrate a general assembly principle of complex communities and provides an appealing explanation for how closely related species are favored during community assembly. Furthermore, the differential regulation of surfactin and bacillaene by the extracellular matrix may explain the spatio-temporal gradients of antibiotic production within biofilms. |
| first_indexed | 2024-04-11T05:20:27Z |
| format | Article |
| id | doaj.art-765bb83e366143c7b67111eb4a013082 |
| institution | Directory Open Access Journal |
| issn | 2001-0370 |
| language | English |
| last_indexed | 2024-04-11T05:20:27Z |
| publishDate | 2022-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Computational and Structural Biotechnology Journal |
| spelling | doaj.art-765bb83e366143c7b67111eb4a0130822022-12-24T04:50:50ZengElsevierComputational and Structural Biotechnology Journal2001-03702022-01-01201525Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community membersHarsh Maan0Tatyana L. Povolotsky1Ziv Porat2Maxim Itkin3Sergey Malitsky4Ilana Kolodkin-Gal5Department of Molecular Genetics, Weizmann Institute of Science, Rehovot, IsraelDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot, IsraelFlow Cytometry Unit, Life Sciences Core Facilities, Weizmann Institute of Science, Rehovot, IsraelLife Science Core Facilities Weizmann Institute of Science, 234 Herzl Street, Rehovot, IsraelLife Science Core Facilities Weizmann Institute of Science, 234 Herzl Street, Rehovot, IsraelDepartment of Molecular Genetics, Weizmann Institute of Science, Rehovot, Israel; Corresponding author.In nature, bacteria frequently reside in differentiated communities or biofilms. These multicellular communities are held together by self-produced polymers that allow the community members to adhere to the surface as well as to neighbor bacteria. Here, we report that exopolysaccharides prevent Bacillus subtilis from co-aggregating with a distantly related bacterium Bacillus mycoides, while maintaining their role in promoting self-adhesion and co-adhesion with phylogenetically related bacterium, Bacillus atrophaeus. The defensive role of the exopolysaccharides is due to the specific regulation of bacillaene. Single cell analysis of biofilm and free-living bacterial cells using imaging flow cytometry confirmed a specific role for the exopolysaccharides in microbial competition repelling B. mycoides. Unlike exopolysaccharides, the matrix protein TasA induced bacillaene but inhibited the expression of the biosynthetic clusters for surfactin, and therefore its overall effect on microbial competition during floating biofilm formation was neutral. Thus, the exopolysaccharides provide a dual fitness advantage for biofilm-forming cells, as it acts to promote co-aggregation of related species, as well as, a secreted cue for chemical interference with non-compatible partners. These results experimentally demonstrate a general assembly principle of complex communities and provides an appealing explanation for how closely related species are favored during community assembly. Furthermore, the differential regulation of surfactin and bacillaene by the extracellular matrix may explain the spatio-temporal gradients of antibiotic production within biofilms.http://www.sciencedirect.com/science/article/pii/S2001037021005080BiofilmsExtracellular matrixImaging flow cytometryGene regulation |
| spellingShingle | Harsh Maan Tatyana L. Povolotsky Ziv Porat Maxim Itkin Sergey Malitsky Ilana Kolodkin-Gal Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members Computational and Structural Biotechnology Journal Biofilms Extracellular matrix Imaging flow cytometry Gene regulation |
| title | Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members |
| title_full | Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members |
| title_fullStr | Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members |
| title_full_unstemmed | Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members |
| title_short | Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members |
| title_sort | imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms to promote self adhesion while repelling non self community members |
| topic | Biofilms Extracellular matrix Imaging flow cytometry Gene regulation |
| url | http://www.sciencedirect.com/science/article/pii/S2001037021005080 |
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