Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing
Life in a three-dimensional biofilm is typical for many bacteria, yet little is known about how strains interact in this context. Here, we created essential gene CRISPR interference knockdown libraries in biofilm-forming Bacillus subtilis and measured competitive fitness during colony co-culture wit...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-02-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/64145 |
| _version_ | 1811180503981621248 |
|---|---|
| author | Heidi A Arjes Lisa Willis Haiwen Gui Yangbo Xiao Jason Peters Carol Gross Kerwyn Casey Huang |
| author_facet | Heidi A Arjes Lisa Willis Haiwen Gui Yangbo Xiao Jason Peters Carol Gross Kerwyn Casey Huang |
| author_sort | Heidi A Arjes |
| collection | DOAJ |
| description | Life in a three-dimensional biofilm is typical for many bacteria, yet little is known about how strains interact in this context. Here, we created essential gene CRISPR interference knockdown libraries in biofilm-forming Bacillus subtilis and measured competitive fitness during colony co-culture with wild type. Partial knockdown of some translation-related genes reduced growth rates and led to out-competition. Media composition led some knockdowns to compete differentially as biofilm versus non-biofilm colonies. Cells depleted for the alanine racemase AlrA died in monoculture but survived in a biofilm colony co-culture via nutrient sharing. Rescue was enhanced in biofilm colony co-culture with a matrix-deficient parent due to a mutualism involving nutrient and matrix sharing. We identified several examples of mutualism involving matrix sharing that occurred in three-dimensional biofilm colonies but not when cultured in two dimensions. Thus, growth in a three-dimensional colony can promote genetic diversity through sharing of secreted factors and may drive evolution of mutualistic behavior. |
| first_indexed | 2024-04-11T09:04:21Z |
| format | Article |
| id | doaj.art-dfad698ad026476980000a45a47b7f4a |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:04:21Z |
| publishDate | 2021-02-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-dfad698ad026476980000a45a47b7f4a2022-12-22T04:32:42ZengeLife Sciences Publications LtdeLife2050-084X2021-02-011010.7554/eLife.64145Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharingHeidi A Arjes0https://orcid.org/0000-0002-4708-4286Lisa Willis1Haiwen Gui2https://orcid.org/0000-0003-0564-940XYangbo Xiao3Jason Peters4Carol Gross5https://orcid.org/0000-0002-5595-9732Kerwyn Casey Huang6https://orcid.org/0000-0002-8043-8138Department of Bioengineering, Stanford University School of Medicine, Stanford, United StatesDepartment of Bioengineering, Stanford University School of Medicine, Stanford, United StatesDepartment of Bioengineering, Stanford University School of Medicine, Stanford, United StatesDepartment of Bioengineering, Stanford University School of Medicine, Stanford, United StatesDepartment of Cell and Tissue Biology, University of California San Francisco, San Francisco, United States; Pharmaceutical Sciences Division, School of Pharmacy, University of Wisconsin-Madison, Madison, United States; Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin-Madison, Madison, United States; Department of Bacteriology, University of Wisconsin-Madison, Madison, United States; Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, United StatesDepartment of Cell and Tissue Biology, University of California San Francisco, San Francisco, United StatesDepartment of Bioengineering, Stanford University School of Medicine, Stanford, United States; Department of Microbiology & Immunology, Stanford University School of Medicine, Stanford, United States; Chan Zuckerberg Biohub, San Francisco, United StatesLife in a three-dimensional biofilm is typical for many bacteria, yet little is known about how strains interact in this context. Here, we created essential gene CRISPR interference knockdown libraries in biofilm-forming Bacillus subtilis and measured competitive fitness during colony co-culture with wild type. Partial knockdown of some translation-related genes reduced growth rates and led to out-competition. Media composition led some knockdowns to compete differentially as biofilm versus non-biofilm colonies. Cells depleted for the alanine racemase AlrA died in monoculture but survived in a biofilm colony co-culture via nutrient sharing. Rescue was enhanced in biofilm colony co-culture with a matrix-deficient parent due to a mutualism involving nutrient and matrix sharing. We identified several examples of mutualism involving matrix sharing that occurred in three-dimensional biofilm colonies but not when cultured in two dimensions. Thus, growth in a three-dimensional colony can promote genetic diversity through sharing of secreted factors and may drive evolution of mutualistic behavior.https://elifesciences.org/articles/64145essential genesCRISPRiAlrAD-alanineextracellular matrixsurface growth |
| spellingShingle | Heidi A Arjes Lisa Willis Haiwen Gui Yangbo Xiao Jason Peters Carol Gross Kerwyn Casey Huang Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing eLife essential genes CRISPRi AlrA D-alanine extracellular matrix surface growth |
| title | Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing |
| title_full | Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing |
| title_fullStr | Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing |
| title_full_unstemmed | Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing |
| title_short | Three-dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing |
| title_sort | three dimensional biofilm colony growth supports a mutualism involving matrix and nutrient sharing |
| topic | essential genes CRISPRi AlrA D-alanine extracellular matrix surface growth |
| url | https://elifesciences.org/articles/64145 |
| work_keys_str_mv | AT heidiaarjes threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing AT lisawillis threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing AT haiwengui threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing AT yangboxiao threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing AT jasonpeters threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing AT carolgross threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing AT kerwyncaseyhuang threedimensionalbiofilmcolonygrowthsupportsamutualisminvolvingmatrixandnutrientsharing |