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Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population

Nature Microbiology volume 1, Article number: 16022 (2016) Cite this article

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Abstract

Ecosystems are highly structured. Organisms are not randomly distributed but can be found in spatial aggregates at many scales, leading to spatial heterogeneity or even regular patterns1. The widespread occurrence of these aggregates in many different ecosystems suggests that generic factors intrinsic to the populations—such as interactions between the organisms—play a major role in their emergence1,2. Beyond the emergence of spatial patchiness, its functional consequences remain unclear. Here we show in Bacillus subtilis that cooperative interactions in a spatial environment are sufficient to form self-organized patches. These patches allow for survival even when the microbe density is too low to sustain growth in a well-mixed environment. Decreasing cell mobility leads to more compact patches that enhance this survival advantage but also reduce the overall growth. Our results highlight that even populations lacking specific group-forming mechanisms can nonetheless form spatial patterns that allow for group survival in challenging environments.

Heterogeneity and spatial patterns can be found in a large variety of microbial ecosystems3–5. Several explanations have been proposed for this heterogeneity, such as selection by locally different environments and colonization, differentiation and extinction dynamics5. However, even for rather homogeneous environments, spatial patterns can be found in bacterial and algal mats, culminating in the complex architecture of stromatolites and microbial reefs6–8. These patterns are often rather periodic and resemble those well known in plants in arid or peatland environments1. For those patterns a major role of intrinsic factors is assumed: they are probably self-organized and cooperative interactions have been suggested to be of importance1,2,9–13; e.g. in arid environments grass may increase the local infiltration of rainwater and thus facilitate growth nearby2. Many microbes are known to show cooperative interactions as a consequence of ‘public good’ production14, raising the question of whether similar mechanisms for pattern formation exist in the microbial realm. Another major question is if there is an ecological benefit from the formation of patterns. Organisms in a group may benefit from each other, but they also experience stronger competition15.

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Figure 1: Cooperative growth in a spatial environment leads to formation of patches.
Figure 2: Self-organized patches allow bacteria to survive lower starting cell densities.
Figure 3: Reaction-diffusion model describes pattern formation.
Figure 4: Trade-off between survival and growth.

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Acknowledgements

We thank D. Kearns, D. Rudner and J. Radeck for generously providing us with strains and plasmids. We thank T. Hugel, I. Bischofs, A. Deutsch, I. Couzin and E. Frey for helpful discussion and all members of the Gore lab for critical reading and discussion of the manuscript. This work was funded by an Allen Distinguished Investigator Award, NSF CAREER Award and NIH New Innovator Award. J.G. is a Pew Scholar in the Biomedical Sciences and a Sloan Fellow.

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  1. Department of Physics Massachusetts Institute of Technology, Physics of Living Systems, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

    Christoph Ratzke & Jeff Gore

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  1. Christoph Ratzke
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  2. Jeff Gore
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Contributions

C.R and J.G. designed the research. C.R. performed the research. C.R. and J.G. wrote the manuscript.

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Correspondence to Christoph Ratzke or Jeff Gore.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Discussion, Figures 1–24 and References (PDF 2245 kb)

Supplementary Video 1

This video is related to Supplementary Fig. 6. At low agar concentrations (0.22%) in the presence of 0.2% fumarate as a carbon source the bacteria are highly mobile. (MP4 336 kb)

Supplementary Video 2

This video is related to Supplementary Fig. 6. At high agar concentrations (1%) in the presence of 0.2% fumarate as a carbon source the bacteria are stalled. (MP4 56 kb)

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Ratzke, C., Gore, J. Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population. Nat Microbiol 1, 16022 (2016). https://doi.org/10.1038/nmicrobiol.2016.22

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