Self-organized canals enable long-range directed material transport in bacterial communities
Curation statements for this article:-
Curated by eLife
Evaluation Summary:
The manuscript describes an interesting phenomenon of long-range transport in self-organized canal structures formed in colonies of the pathogenic bacterium Pseudomonas aeruginosa. The authors measured and analyzed the fluid flows in these open channels, revealing that it is capable of supporting high-speed transport of outer membrane vesicles and bacterial cells over centimeters. This study sheds new light on the potential amplitude of cargo exchange among bacterial communities over long distances.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (eLife)
- Structural Biology and Molecular Biophysics (eLife)
Abstract
Long-range material transport is essential to maintain the physiological functions of multicellular organisms such as animals and plants. By contrast, material transport in bacteria is often short-ranged and limited by diffusion. Here, we report a unique form of actively regulated long-range directed material transport in structured bacterial communities. Using Pseudomonas aeruginosa colonies as a model system, we discover that a large-scale and temporally evolving open-channel system spontaneously develops in the colony via shear-induced banding. Fluid flows in the open channels support high-speed (up to 450 µm/s) transport of cells and outer membrane vesicles over centimeters, and help to eradicate colonies of a competing species Staphylococcus aureus . The open channels are reminiscent of human-made canals for cargo transport, and the channel flows are driven by interfacial tension mediated by cell-secreted biosurfactants. The spatial-temporal dynamics of fluid flows in the open channels are qualitatively described by flow profile measurement and mathematical modeling. Our findings demonstrate that mechanochemical coupling between interfacial force and biosurfactant kinetics can coordinate large-scale material transport in primitive life forms, suggesting a new principle to engineer self-organized microbial communities.
Article activity feed
-
-
Author Response
Reviewer #1 (Public Review):
A limitation here is that this colony morphology only seems to manifest strongly in mutants lacking flagella, which I don't think is common among wild P. aeruginosa isolates. To the extent that groups of P. aeruginosa cells have been imaged in situ, e.g. in the sputum of CF patients, this kind of channel formation does not occur in more realistic conditions. See DePas et al. (2015) https://journals.asm.org/doi/epub/10.1128/mBio.00796-16. I think it's more likely that this colony morphology is idiosyncratic to the agar growth substrate on which the cells are growing in this case, so the more interesting thing here is the physics of the system rather than its applications to clinical or ecological settings.
We thank the Reviewer for appreciating the novelty of our work. We have revised the …
Author Response
Reviewer #1 (Public Review):
A limitation here is that this colony morphology only seems to manifest strongly in mutants lacking flagella, which I don't think is common among wild P. aeruginosa isolates. To the extent that groups of P. aeruginosa cells have been imaged in situ, e.g. in the sputum of CF patients, this kind of channel formation does not occur in more realistic conditions. See DePas et al. (2015) https://journals.asm.org/doi/epub/10.1128/mBio.00796-16. I think it's more likely that this colony morphology is idiosyncratic to the agar growth substrate on which the cells are growing in this case, so the more interesting thing here is the physics of the system rather than its applications to clinical or ecological settings.
We thank the Reviewer for appreciating the novelty of our work. We have revised the third paragraph of Discussion section to limit the generality of our findings in clinical or ecological settings (lines 440-456). Results of imaging P. aeruginosa cells in situ in sputum samples from cystic fibrosis patients are compared, and the shortage of using flagellum mutants is highlighted.
The authors have established that flgK-null P. aeruginosa forms colonies with channels in this agar growth and incubation environment, and made a strong case for the physics underlying the spontaneous formation of this morphology. The idea that this morphology reflects a multicellular developmental program for P. aeruginosa is not strong, though, as this morphology is not found in the wild. In general, the idea that groups of microbes on agar are analogous to multicellular organisms with circulatory systems has little support from in-situ imaging experiments, or from fundamental evolutionary theory. So, I would advise shifting the introduction and discussion away from the multicellular organism focus toward a greater focus on the physics of the system and its potential for synthetic systems. See for example Yan et al. (2019) https://elifesciences.org/articles/43920
We thank the Reviewer for the suggestion. We now focus more on the physics of canal formation in Introduction and Discussion (revising/adding texts in lines 93-99 and restructuring the paragraphs in Discussion section). We also put greater emphasis on the application of our findings for engineering living materials based on synthetic microbial consortia (lines 58-64, 428-438), while deleting the texts related to the implication for multicellularity in Introduction/Discussion.
-
Evaluation Summary:
The manuscript describes an interesting phenomenon of long-range transport in self-organized canal structures formed in colonies of the pathogenic bacterium Pseudomonas aeruginosa. The authors measured and analyzed the fluid flows in these open channels, revealing that it is capable of supporting high-speed transport of outer membrane vesicles and bacterial cells over centimeters. This study sheds new light on the potential amplitude of cargo exchange among bacterial communities over long distances.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
-
Reviewer #1 (Public Review):
This project by Li et al. describes a colony morphology of P. aeruginosa that arises on agar plates and is especially pronounced in mutants lacking flagella, which were used for the majority of experiments in the paper. The paper documents the formation of large channels in the projections of swarming colonies, and within these channels, the rapid transport of fluid, cells, and extracellular vesicles. This transport is measured with great care and supported with additional support modeling.
- By and large, the project looks to have been executed with strong methodology and attention to detail in describing the channel formation effect found among colonies of P. aeruginosa flgK mutants. The authors have done very well in pushing known imaging methods to document transport within the colony channels and to …
Reviewer #1 (Public Review):
This project by Li et al. describes a colony morphology of P. aeruginosa that arises on agar plates and is especially pronounced in mutants lacking flagella, which were used for the majority of experiments in the paper. The paper documents the formation of large channels in the projections of swarming colonies, and within these channels, the rapid transport of fluid, cells, and extracellular vesicles. This transport is measured with great care and supported with additional support modeling.
- By and large, the project looks to have been executed with strong methodology and attention to detail in describing the channel formation effect found among colonies of P. aeruginosa flgK mutants. The authors have done very well in pushing known imaging methods to document transport within the colony channels and to make a case for how this transport is being driven physically. I think the aims of the detailed description of the physical phenomenon of colony growth in this environmental condition have been accomplished.
- A limitation here is that this colony morphology only seems to manifest strongly in mutants lacking flagella, which I don't think is common among wild P. aeruginosa isolates. To the extent that groups of P. aeruginosa cells have been imaged in situ, e.g. in the sputum of CF patients, this kind of channel formation does not occur in more realistic conditions. See DePas et al. (2015) https://journals.asm.org/doi/epub/10.1128/mBio.00796-16. I think it's more likely that this colony morphology is idiosyncratic to the agar growth substrate on which the cells are growing in this case, so the more interesting thing here is the physics of the system rather than its applications to clinical or ecological settings.
- The authors have established that flgK-null P. aeruginosa forms colonies with channels in this agar growth and incubation environment, and made a strong case for the physics underlying the spontaneous formation of this morphology. The idea that this morphology reflects a multicellular developmental program for P. aeruginosa is not strong, though, as this morphology is not found in the wild. In general, the idea that groups of microbes on agar are analogous to multicellular organisms with circulatory systems has little support from in-situ imaging experiments, or from fundamental evolutionary theory. So, I would advise shifting the introduction and discussion away from the multicellular organism focus toward a greater focus on the physics of the system and its potential for synthetic systems. See for example Yan et al. (2019) https://elifesciences.org/articles/43920
-
Reviewer #2 (Public Review):
In this work, Li and colleagues describe a very interesting discovery on the long-range transport in self-organized canals in Pseudomonas colonies. Briely, during the development of a Pseudomonas colony, bacterial canals would form in colony branches, in major part driven by rhamnolipids (a surfactant) produced by Pseudomonas. In each canal, there's a gradient of surface tension, created by the surfactant. The gradient can drive the extremely rapid transport of cells and particles. The quantitative features of the transport dynamics can be captured by a hydrodynamic model.
Overall, I find this to be an extremely interesting discovery, which may play a critical role in the development of branching patterns in Pseudomonas. As far as I know, the unique features of Pseudomonas branching pattern formation are not …
Reviewer #2 (Public Review):
In this work, Li and colleagues describe a very interesting discovery on the long-range transport in self-organized canals in Pseudomonas colonies. Briely, during the development of a Pseudomonas colony, bacterial canals would form in colony branches, in major part driven by rhamnolipids (a surfactant) produced by Pseudomonas. In each canal, there's a gradient of surface tension, created by the surfactant. The gradient can drive the extremely rapid transport of cells and particles. The quantitative features of the transport dynamics can be captured by a hydrodynamic model.
Overall, I find this to be an extremely interesting discovery, which may play a critical role in the development of branching patterns in Pseudomonas. As far as I know, the unique features of Pseudomonas branching pattern formation are not well understood. Typical reactive diffusion models have not been able to explain the thin branches Pseudomonas colonies often develop. Perhaps, the long-range, rapid transport of cells through bacterial canals described here could provide a critical piece that's missing in the past mechanistic models of Pseudomonas branching dynamics.
My impression is that the results are quite convincing and the experiments and modeling are rigorously carried out. I should note that many of the quantitative measurements described are quite challenging to conduct, and require meticulous imaging and data analysis (in addition to proper microbiology experiments). Likewise, the formulation and analysis of the presented model (in a way that's mapped to the quantitative experiments) are highly non-trivial.
-
