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...

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Autores principales: Aimee K. Wessel, Talha A. Arshad, Mignon Fitzpatrick, Jodi L. Connell, Roger T. Bonnecaze, Jason B. Shear, Marvin Whiteley
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:a037e6ccbf604edf85651ed8db0e87052021-11-15T15:45:13ZOxygen Limitation within a Bacterial Aggregate10.1128/mBio.00992-142150-7511https://doaj.org/article/a037e6ccbf604edf85651ed8db0e87052014-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00992-14https://doaj.org/toc/2150-7511ABSTRACT 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.Aimee K. WesselTalha A. ArshadMignon FitzpatrickJodi L. ConnellRoger T. BonnecazeJason B. ShearMarvin WhiteleyAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 2 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
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
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.
format article
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
title Oxygen Limitation within a Bacterial Aggregate
title_short 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_sort oxygen limitation within a bacterial aggregate
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/a037e6ccbf604edf85651ed8db0e8705
work_keys_str_mv AT aimeekwessel oxygenlimitationwithinabacterialaggregate
AT talhaaarshad oxygenlimitationwithinabacterialaggregate
AT mignonfitzpatrick oxygenlimitationwithinabacterialaggregate
AT jodilconnell oxygenlimitationwithinabacterialaggregate
AT rogertbonnecaze oxygenlimitationwithinabacterialaggregate
AT jasonbshear oxygenlimitationwithinabacterialaggregate
AT marvinwhiteley oxygenlimitationwithinabacterialaggregate
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