Dynamic interspecies interactions and robustness in a four‐species model biofilm
Abstract Interspecific interactions within biofilms determine relative species abundance, growth dynamics, community resilience, and success or failure of invasion by an extraneous organism. However, deciphering interspecific interactions and assessing their contribution to biofilm properties and fu...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2021-12-01
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| Series: | MicrobiologyOpen |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/mbo3.1254 |
| _version_ | 1819278294969745408 |
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| author | Aurélie Baliarda Michèle Winkler Laurent Tournier Colin R. Tinsley Stéphane Aymerich |
| author_facet | Aurélie Baliarda Michèle Winkler Laurent Tournier Colin R. Tinsley Stéphane Aymerich |
| author_sort | Aurélie Baliarda |
| collection | DOAJ |
| description | Abstract Interspecific interactions within biofilms determine relative species abundance, growth dynamics, community resilience, and success or failure of invasion by an extraneous organism. However, deciphering interspecific interactions and assessing their contribution to biofilm properties and function remain a challenge. Here, we describe the constitution of a model biofilm composed of four bacterial species belonging to four different genera (Rhodocyclus sp., Pseudomonas fluorescens, Kocuria varians, and Bacillus cereus), derived from a biofilm isolated from an industrial milk pasteurization unit. We demonstrate that the growth dynamics and equilibrium composition of this biofilm are highly reproducible. Based on its equilibrium composition, we show that the establishment of this four‐species biofilm is highly robust against initial, transient perturbations but less so towards continuous perturbations. By comparing biofilms formed from different numbers and combinations of the constituent species and by fitting a growth model to the experimental data, we reveal a network of dynamic, positive, and negative interactions that determine the final composition of the biofilm. Furthermore, we reveal that the molecular determinant of one negative interaction is the thiocillin I synthesized by the B. cereus strain, and demonstrate its importance for species distribution and its impact on robustness by mutational analysis of the biofilm ecosystem. |
| first_indexed | 2024-12-24T00:09:44Z |
| format | Article |
| id | doaj.art-f5fe999828e94835ae61560a37fab0e0 |
| institution | Directory Open Access Journal |
| issn | 2045-8827 |
| language | English |
| last_indexed | 2024-12-24T00:09:44Z |
| publishDate | 2021-12-01 |
| publisher | Wiley |
| record_format | Article |
| series | MicrobiologyOpen |
| spelling | doaj.art-f5fe999828e94835ae61560a37fab0e02022-12-21T17:24:55ZengWileyMicrobiologyOpen2045-88272021-12-01106n/an/a10.1002/mbo3.1254Dynamic interspecies interactions and robustness in a four‐species model biofilmAurélie Baliarda0Michèle Winkler1Laurent Tournier2Colin R. Tinsley3Stéphane Aymerich4INRAE, AgroParisTech, Micalis Institute Université Paris‐Saclay Jouy‐en‐Josas FranceINRAE, AgroParisTech, Micalis Institute Université Paris‐Saclay Jouy‐en‐Josas FranceINRAE, MaIAGE Université Paris‐Saclay Jouy‐en‐Josas FranceINRAE, AgroParisTech, Micalis Institute Université Paris‐Saclay Jouy‐en‐Josas FranceINRAE, AgroParisTech, Micalis Institute Université Paris‐Saclay Jouy‐en‐Josas FranceAbstract Interspecific interactions within biofilms determine relative species abundance, growth dynamics, community resilience, and success or failure of invasion by an extraneous organism. However, deciphering interspecific interactions and assessing their contribution to biofilm properties and function remain a challenge. Here, we describe the constitution of a model biofilm composed of four bacterial species belonging to four different genera (Rhodocyclus sp., Pseudomonas fluorescens, Kocuria varians, and Bacillus cereus), derived from a biofilm isolated from an industrial milk pasteurization unit. We demonstrate that the growth dynamics and equilibrium composition of this biofilm are highly reproducible. Based on its equilibrium composition, we show that the establishment of this four‐species biofilm is highly robust against initial, transient perturbations but less so towards continuous perturbations. By comparing biofilms formed from different numbers and combinations of the constituent species and by fitting a growth model to the experimental data, we reveal a network of dynamic, positive, and negative interactions that determine the final composition of the biofilm. Furthermore, we reveal that the molecular determinant of one negative interaction is the thiocillin I synthesized by the B. cereus strain, and demonstrate its importance for species distribution and its impact on robustness by mutational analysis of the biofilm ecosystem.https://doi.org/10.1002/mbo3.1254adhesionbiofilmmicrobial ecologymicrobial interactions and pathogenesis |
| spellingShingle | Aurélie Baliarda Michèle Winkler Laurent Tournier Colin R. Tinsley Stéphane Aymerich Dynamic interspecies interactions and robustness in a four‐species model biofilm MicrobiologyOpen adhesion biofilm microbial ecology microbial interactions and pathogenesis |
| title | Dynamic interspecies interactions and robustness in a four‐species model biofilm |
| title_full | Dynamic interspecies interactions and robustness in a four‐species model biofilm |
| title_fullStr | Dynamic interspecies interactions and robustness in a four‐species model biofilm |
| title_full_unstemmed | Dynamic interspecies interactions and robustness in a four‐species model biofilm |
| title_short | Dynamic interspecies interactions and robustness in a four‐species model biofilm |
| title_sort | dynamic interspecies interactions and robustness in a four species model biofilm |
| topic | adhesion biofilm microbial ecology microbial interactions and pathogenesis |
| url | https://doi.org/10.1002/mbo3.1254 |
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