Oxygen Limitation within a Bacterial Aggregate
ABSTRACT Cells within biofilms exhibit physiological heterogeneity, in part because of chemical gradients existing within these spatially structured communities. Previous work has examined how chemical gradients develop in large biofilms containing >108 cells. However, many bacterial communities...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2014-05-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00992-14 |
| _version_ | 1818822511670853632 |
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| author | Aimee K. Wessel Talha A. Arshad Mignon Fitzpatrick Jodi L. Connell Roger T. Bonnecaze Jason B. Shear Marvin Whiteley |
| author_facet | Aimee K. Wessel Talha A. Arshad Mignon Fitzpatrick Jodi L. Connell Roger T. Bonnecaze Jason B. Shear Marvin Whiteley |
| author_sort | Aimee K. Wessel |
| collection | DOAJ |
| description | ABSTRACT Cells within biofilms exhibit physiological heterogeneity, in part because of chemical gradients existing within these spatially structured communities. Previous work has examined how chemical gradients develop in large biofilms containing >108 cells. However, many bacterial communities in nature are composed of small, densely packed aggregates of cells (≤105 bacteria). Using a gelatin-based three-dimensional (3D) printing strategy, we confined the bacterium Pseudomonas aeruginosa within picoliter-sized 3D “microtraps” that are permeable to nutrients, waste products, and other bioactive small molecules. We show that as a single bacterium grows into a maximally dense (1012 cells ml−1) clonal population, a localized depletion of oxygen develops when it reaches a critical aggregate size of ~55 pl. Collectively, these data demonstrate that chemical and phenotypic heterogeneity exists on the micrometer scale within small aggregate populations. IMPORTANCE Before developing into large, complex communities, microbes initially cluster into aggregates, and it is unclear if chemical heterogeneity exists in these ubiquitous micrometer-scale aggregates. We chose to examine oxygen availability within an aggregate since oxygen concentration impacts a number of important bacterial processes, including metabolism, social behaviors, virulence, and antibiotic resistance. By determining that oxygen availability can vary within aggregates containing ≤105 bacteria, we establish that physiological heterogeneity exists within P. aeruginosa aggregates, suggesting that such heterogeneity frequently exists in many naturally occurring small populations. |
| first_indexed | 2024-12-18T23:25:15Z |
| format | Article |
| id | doaj.art-a037e6ccbf604edf85651ed8db0e8705 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T23:25:15Z |
| publishDate | 2014-05-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-a037e6ccbf604edf85651ed8db0e87052022-12-21T20:47:49ZengAmerican Society for MicrobiologymBio2150-75112014-05-015210.1128/mBio.00992-14Oxygen Limitation within a Bacterial AggregateAimee K. Wessel0Talha A. Arshad1Mignon Fitzpatrick2Jodi L. Connell3Roger T. Bonnecaze4Jason B. Shear5Marvin Whiteley6Department of Molecular Biosciences, University of Texas at Austin, Austin, Texas, USADepartment of Chemical Engineering, University of Texas at Austin, Austin, Texas, USADepartment of Chemistry and Biochemistry, University of Texas at Austin, Austin, Texas, USADepartment of Molecular Biosciences, University of Texas at Austin, Austin, Texas, USADepartment of Chemical Engineering, University of Texas at Austin, Austin, Texas, USADepartment of Chemistry and Biochemistry, University of Texas at Austin, Austin, Texas, USADepartment of Molecular Biosciences, University of Texas at Austin, Austin, Texas, USAABSTRACT Cells within biofilms exhibit physiological heterogeneity, in part because of chemical gradients existing within these spatially structured communities. Previous work has examined how chemical gradients develop in large biofilms containing >108 cells. However, many bacterial communities in nature are composed of small, densely packed aggregates of cells (≤105 bacteria). Using a gelatin-based three-dimensional (3D) printing strategy, we confined the bacterium Pseudomonas aeruginosa within picoliter-sized 3D “microtraps” that are permeable to nutrients, waste products, and other bioactive small molecules. We show that as a single bacterium grows into a maximally dense (1012 cells ml−1) clonal population, a localized depletion of oxygen develops when it reaches a critical aggregate size of ~55 pl. Collectively, these data demonstrate that chemical and phenotypic heterogeneity exists on the micrometer scale within small aggregate populations. IMPORTANCE Before developing into large, complex communities, microbes initially cluster into aggregates, and it is unclear if chemical heterogeneity exists in these ubiquitous micrometer-scale aggregates. We chose to examine oxygen availability within an aggregate since oxygen concentration impacts a number of important bacterial processes, including metabolism, social behaviors, virulence, and antibiotic resistance. By determining that oxygen availability can vary within aggregates containing ≤105 bacteria, we establish that physiological heterogeneity exists within P. aeruginosa aggregates, suggesting that such heterogeneity frequently exists in many naturally occurring small populations.https://journals.asm.org/doi/10.1128/mBio.00992-14 |
| spellingShingle | Aimee K. Wessel Talha A. Arshad Mignon Fitzpatrick Jodi L. Connell Roger T. Bonnecaze Jason B. Shear Marvin Whiteley Oxygen Limitation within a Bacterial Aggregate mBio |
| title | Oxygen Limitation within a Bacterial Aggregate |
| title_full | Oxygen Limitation within a Bacterial Aggregate |
| title_fullStr | Oxygen Limitation within a Bacterial Aggregate |
| title_full_unstemmed | Oxygen Limitation within a Bacterial Aggregate |
| title_short | Oxygen Limitation within a Bacterial Aggregate |
| title_sort | oxygen limitation within a bacterial aggregate |
| url | https://journals.asm.org/doi/10.1128/mBio.00992-14 |
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