- Open Access
Bacterial Route Finding and Collective Escape in Mazes and Fractals
Phys. Rev. X 10, 031017 – Published 22 July, 2020
DOI: https://doi.org/10.1103/PhysRevX.10.031017
Abstract
Bacteria which grow not on the featureless agar plates of the microbiology lab but in the real world must navigate topologies which are nontrivially complex, such as mazes or fractals. We show that chemosensitive motile E. coli can efficiently explore nontrivial mazes in times much shorter than a no-memory (Markovian) walk would predict, and can collectively escape from a fractal topology. The strategies used by the bacteria include individual power-law probability distribution function exploration, the launching of chemotactic collective waves with preferential branching at maze nodes and defeating of fractal pumping, and bet hedging in case the more risky attempts to find food fail.
Physics Subject Headings (PhySH)
Popular Summary
Bacteria outside of the lab must often navigate complex environments in search of food. A better understanding of how bacteria find their way might help researchers develop strategies to inhibit bacterial infections. To that end, we probe to what extent the common bacteria E. coli explores landscapes that have much in common with structures experienced in nature—fractals and mazes—and find that they appear to have evolved a variety of ways to navigate these puzzles.
Fractals are scale-free topologies that repeat themselves with increasing magnification. A maze is not scale free but has many possible paths, with some leading quickly to an exit and others requiring a much longer time. While our designed puzzles seem simplistic, we aim to capture the essence of how bacteria navigate and escape more complex structures and reveal the emergent collective behavior of challenges to survival. For both types of puzzles, the bacteria employ several strategies to efficiently explore the territory, escaping in less time than would be expected if the bacteria moved randomly.
We caution that there are many aspects of these experiments we do not yet understand. In microbiology research, control experiments are difficult because one often must resort to controls using different strains of bacteria, which may have their own altered (unexpected) behavior. We believe that the phenomena we see are emergent: They cannot be easily predicted from a bottoms-up approach and they might not appear if the bacteria are not presented with a similar challenge.
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References (32)
- E. Shimon, Graph Algorithms, 2nd ed. (Cambridge University Press, Cambridge, 2011).
- H. C. Berg, Random Walks in Biology (Princeton University Press, Princeton, 1983).
- S. Lorthois and F. Cassot, Fractal Analysis of Vascular Networks: Insights from Morphogenesis, J. Theor. Biol. 262, 614 (2010).
- M. Saar, T. Gilad, T. Kilon-Kallner, A. Rosenfeld, A. Subach, and I. Scharf, The Interplay between Maze Complexity, Colony Size, Learning and Memory in Ants While Solving a Maze: A Test at the Colony Level, PLoS One 12, e0183753 (2017).
- Q. Zhang, G. Lambert, D. Liao, H. Kim, K. Robin, C. K. Tung, N. Pourmand, and R. H. Austin, Acceleration of Emergence of Bacterial Antibiotic Resistance in Connected Microenvironments, Science 333, 1764 (2011).
- F. E. Lennon, G. C. Cianci, N. A. Cipriani, T. A. Hensing, H. J. Zhang, C. T. Chen, S. D. Murgu, E. E. Vokes, M. W. Vannier, and R. Salgia, Lung Cancer—A Fractal Viewpoint, Nat. Rev. Clin. Oncol. 12, 664 (2015).
- E. Mathieu, U. Escribano-Vazquez, D. Descamps, C. Cherbuy, P. Langella, S. Riffault, A. Remot, and M. Thomas, Paradigms of Lung Microbiota Functions in Health and Disease, Particularly, in Asthma, Front. Physiol. 9, 1168 (2018).
- Z. T. Zhou, T. Zhou, S. Q. Zhang, Z. F. Shi, Y. Chen, W. J. Wan, X. X. Li, X. Z. Chen, S. N. G. Corder, Z. L. Fu, L. Chen, Y. Mao, J. C. Cao, F. G. Omenetto, M. K. Liu, H. Li, and T. H. Tao, Multicolor -Ray Imaging Using Multispectral Metamaterials, Adv. Sci. 5, 1700982 (2018).
- F. Viela, M. Mathelie-Guinlet, A. Viljoen, and Y. F. Dufrene, What Makes Bacterial Pathogens So Sticky? Mol. Microbiol. 113, 683 (2020).
- Marcos, H. C. Fu, T. R. Powers, and R. Stocker, Bacterial Rheotaxis, Proc. Natl. Acad. Sci. U.S.A. 109, 4780 (2012).
- See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevX.10.031017 for video smovie 1: Bacteria in a nontrivial topology maze, with a very small hydrodynamic outflow; for video smovie-2: Bacteria in a nontrivial topology maze, with a very small hydrodynamic inflow; for video smovie-3: Bacteria in a fractal environment; for video smovie-4: Comparison between the behavior of chemotactic and nonchemotactic bacteria in a fractal environment; for video smovie-5: A random-walk simulation of the bacteria in a fractal environment; and for video smovie-6: Bacteria in a trivial maze (one short path and one long path to the food source, the rest are dead ends), where the connected habitats are of the same size (the scale factor is ).
- T. R. Maarleveld, B. G. Olivier, and F. J. Bruggeman, stochpy: A Comprehensive, User-Friendly Tool for Simulating Stochastic Biological Processes, PLoS One 8, e79345 (2013).
- K. Nagy, O. Sipos, S. Valkai, E. Gombai, O. Hodula, A. Kerenyi, P. Ormos, and P. Galajda, Microfluidic Study of the Chemotactic Response of Escherichia Coli to Amino Acids, Signaling Molecules and Secondary Metabolites, Biomicrofluidics 9, 044105 (2015).
- F. Matthaus, M. Jagodic, and J. Dobnikar, E. Coli Superdiffusion and Chemotaxis-Search Strategy, Precision, and Motility, Biophys. J. 97, 946 (2009).
- F. Detcheverry, Generalized Run-and-Turn Motions: From Bacteria to Lévy Walks, Phys. Rev. E 96, 012415 (2017).
- R. H. Austin, K. Beeson, L. Eisenstein, H. Frauenfelder, I. C. Gunsalus, and V. P. Marshall, Dynamics of Carbon Monoxide Binding by Heme Proteins, Science 181, 541 (1973).
- X. Fu, S. Kato, J. Long, H. H. Mattingly, C. He, D. C. Vural, S. W. Zucker, and T. Emonet, Spatial Self-Organization Resolves Conflicts between Individuality and Collective Migration, Nat. Commun. 9, 2177 (2018).
- H. Mattingly and T. Emonet, The Balancing Act of Growth and Expansion, Nature (London) 575, 602 (2019).
- J. Cremer, T. Honda, Y. Tang, J. Wong-Ng, M. Vergassola, and T. Hwa, Chemotaxis as a Navigation Strategy to Boost Range Expansion, Nature (London) 575, 658 (2019).
- O. Steinbock, A. Toth, and K. Showalter, Navigating Complex Labyrinths: Optimal Paths from Chemical Waves, Science 267, 868 (1995).
- K. J. Painter, Mathematical Models for Chemotaxis and Their Applications in Self-Organisation Phenomena, J. Theor. Biol. 481, 162 (2019).
- H. M. Byrne and M. R. Owen, A New Interpretation of the Keller-Segel Model Based on Multiphase Modeling, J. Math. Biol. 49, 604 (2004).
- M. P. Brenner, L. S. Levitov, and E. O. Budrene, Physical Mechanisms for Chemotactic Pattern Formation by Bacteria, Biophys. J. 74, 1677 (1998).
- G. B. Zhang and X. Q. Zhao, Propagation Dynamics of a Nonlocal Dispersal Fisher-KPP Equation in a Time-Periodic Shifting Habitat, J. Differ. Eq. 268, 2852 (2020).
- Y. H. Tu, Quantitative Modeling of Bacterial Chemotaxis: Signal Amplification and Accurate Adaptation, Ann. Rev. Biophys. 42, 337 (2013).
- H. C. Berg, E. Coli in Motion (Springer Science & Business Media, Berlin, Heidelberg, 2008).
- K. Falconer, Fractal Geometry: Mathematical Foundations and Applications (John Wiley & Sons, New York, 2004).
- C. S. Patlak, The Effect of the Previous Generation on the Distribution of Gene Frequencies in Populations, Proc. Natl. Acad. Sci. U.S.A. 39, 1063 (1953).
- E. F. Keller and L. A. Segel, Initiation of Slime Mold Aggregation Viewed as an Instability, J. Theor. Biol. 26, 399 (1970).
- S. Park, P. M. Wolanin, E. A. Yuzbashyan, H. Lin, N. C. Darnton, J. B. Stock, P. Silberzan, and R. Austin, Influence of Topology on Bacterial Social Interaction, Proc. Natl. Acad. Sci. U.S.A. 100, 13910 (2003).
