Bacterial community morphogenesis is intimately linked to the intracellular redox state
Open accessAbstract
Many microbial species form multicellular structures comprising elaborate wrinkles and concentric rings, yet the rules governing their architecture are poorly understood. The opportunistic pathogen Pseudomonas aeruginosa produces phenazines, small molecules that act as alternate electron acceptors to oxygen and nitrate to oxidize the intracellular redox state and that influence biofilm morphogenesis. Here, we show that the depth occupied by cells within colony biofilms correlates well with electron acceptor availability. Perturbations in the environmental provision, endogenous production, and utilization of electron acceptors affect colony development in a manner consistent with redox control. Intracellular NADH levels peak before the induction of colony wrinkling. These results suggest that redox imbalance is a major factor driving the morphogenesis of P. aeruginosa biofilms and that wrinkling itself is an adaptation that maximizes oxygen accessibility and thereby supports metabolic homeostasis. This type of redox-driven morphological change is reminiscent of developmental processes that occur in metazoans.
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In Pseudomonas aeruginosa, wrinkled colony morphology is a redox-driven adaptation that maximizes oxygen accessibility and increased oxygen inhibits wrinkle formation.
“In the bacterium Pseudomonas aeruginosa wrinkled colony morphology has been shown to be a redox-driven adaptation that maximizes oxygen accessibility and increased oxygen is able to inhibit wrinkle formation [69].”
From Mitochondrial Activity and Cyr1 Are Key Regulators of Ras1 Activation of C. albicans Virulence Pathways (2015) · cites this paper as [69]
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“Oxygen limitation was previously shown to have a pivotal role in wrinkles formation by several bacteria.(17,55,56) We have shown that endogenous accumulation of carbon dioxide and calcium availability serve as an additional signal for extracellular matrix production.”
BackgroundGrahl, N., Demers, E. G., Lindsay, A. K., Harty, C. E., Willger, S. D., Piispanen, A. E., & Hogan, D. A. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1005133 · Cited by 111 · see citing works
“aeruginosa wrinkled colony morphology has been shown to be a redox-driven adaptation that maximizes oxygen accessibility and increased oxygen is able to inhibit wrinkle formation [69].”
Background
- Authors
- Dietrich, L. E. P., Okegbe, C., Price-Whelan, A., Sakhtah, H., Hunter, R. C., & Newman, D. K.
- Affiliations
- Howard Hughes Medical Institute (US)
- Columbia University (US)
- Department of Biology and Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
- California Institute of Technology (US)
- Venue
- Journal of Bacteriology
- Publisher
- American Society for Microbiology
- Published
- 2013-04
- Volume
- 195
- Issue
- 7
- Pages
- 1371-1380
- ISSN
- 0021-9193 (ISSN-L)
- 1098-5530
- PMC
- PMC3624522
- OpenAlex
- W2104767186
- Cited by
- 291
- References
- 44
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 13 · 2023: 26 · 2022: 19 · 2021: 29 · 2020: 27 · 2019: 19 · 2018: 27 · 2017: 31 · 2016: 21 · 2015: 15 · 2014: 21 · 2013: 14
- FWCI
- 10.61
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Bacteriology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Columbia Academic Commons (Columbia University)
- Funders
- National Science Foundation
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Physical Sciences › Environmental Science › Environmental Engineering › Microbial Fuel Cells and Bioremediation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Pseudomonas aeruginosa, phenazine, cellular redox state, NADH, electron acceptors, metabolic homeostasis, bacterial development
- MeSH terms
- Cytoplasm, NAD, Oxidation-Reduction, Phenazines, Pseudomonas aeruginosa, Biofilms
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