- Open Access
Density-controlled reversal of collective migration in bacterial aerotaxis
Phys. Rev. Research 8, 033059 – Published 14 July, 2026
DOI: https://doi.org/10.1103/y7l1-288v
Abstract
In living matter, chemical gradients that populations generate and reshape often guide collective migration. Bacterial aerotaxis exemplifies this feedback between metabolism and movement, giving rise to unexpected collective behaviors. Here, we combine quantitative experiments, theoretical modeling, and numerical simulations to reveal a striking, density-dependent reversal in the migration of Escherichia coli within self-generated oxygen gradients. At low cell densities, populations retreat from the oxygen-rich interface; at high densities, they move toward it. A biophysical model in which bacteria bias their motion toward an intermediate, metabolically optimal oxygen concentration quantitatively captures this reversal and predicts a critical density at which collective migration ceases, even in the presence of sustained oxygen gradients. These findings reconcile long-standing discrepancies in observations of bacterial aerotaxis and highlight how feedback between metabolism, movement, and environmental shaping governs emergent behaviors in active matter, with potential implications for microbiome ecology.
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References (63)
- S. C. Takatori, T. Quah, and J. B. Rawlings, Feedback control of active matter, Annu. Rev. Condens. Matter Phys. 16, 319 (2025).
- A. Gelimson, K. Zhao, C. K. Lee, W. T. Kranz, G. C. L. Wong, and R. Golestanian, Multicellular self-organization of P. aeruginosa due to interactions with secreted trails, Phys. Rev. Lett. 117, 178102 (2016).
- F. L. Memarian, J. D. Lopes, F. J. Schwarzendahl, M. G. Athani, N. Sarpangala, A. Gopinathan, D. A. Beller, K. Dasbiswas, and L. S. Hirst, Active nematic order and dynamic lane formation of microtubules driven by membrane-bound diffusing motors, Proc. Natl. Acad. Sci. USA 118, e2117107118 (2021).
- R. M. Adar and J.-F. Joanny, Environment-stored memory in active nematics and extra-cellular matrix remodeling, Phys. Rev. Lett. 133, 118402 (2024).
- G. H. Wadhams and J. P. Armitage, Making sense of it all: Bacterial chemotaxis, Nat. Rev. Mol. Cell. Biol. 5, 1024 (2004).
- V. Sourjik and N. S. Wingreen, Responding to chemical gradients: Bacterial chemotaxis, Curr. Opin. Cell Biol. 24, 262 (2012).
- S. Park, P. M. Wolanin, E. A. Yuzbashyan, P. Silberzan, J. B. Stock, and R. H. Austin, Motion to form a quorum, Science 301, 188 (2003).
- J. Adler, Chemotaxis in bacteria: Motile Escherichia coli migrate in bands that are influenced by oxygen and organic nutrients, Science 153, 708 (1966).
- E. O. Budrene and H. C. Berg, Complex patterns formed by motile cells of Escherichia coli, Nature (London) 349, 630 (1991).
- E. Lushi, R. E. Goldstein, and M. J. Shelley, Collective chemotactic dynamics in the presence of self-generated fluid flows, Phys. Rev. E 86, 040902(R) (2012).
- T. W. Engelmann, Neue methode zur untersuchung der sauerstoffausscheidung pflanzlicher und thierischer organismen, Pflügers Archiv. 25, 285 (1881).
- W. Pfeffer, Locomotorische richtungsbewegungen durch chemische reize, Untersuch. Botan. Inst. Tübingen 1, 363 (1884).
- W. Pfeffer, Über chemotaktische bewegungen von bacterien, flagellaten und volvocineen, Untersuch. Botan. Inst. Tübingen 2, 582 (1888).
- T. Fenchel, G. King, and T. Blackburn, Bacterial Biogeochemistry: The Ecophysiology of Mineral Cycling, 3rd ed. (Elsevier, Amsterdam, 2012).
- G. Gottschalk, Bacterial Metabolism, 2nd ed. (Springer, New York, 1986).
- D. Saintillan and M. J. Shelley, Theory of active suspensions, in Complex Fluids in Biological Systems: Experiment, Theory, and Computation, edited by S. E. Spagnolie (Springer, New York, 2015), pp. 319–355.
- I. S. Aranson, Bacterial active matter, Rep. Prog. Phys. 85, 076601 (2022).
- F. Menolascina, R. Rusconi, V. I. Fernandez, S. Smriga, Z. Aminzare, E. D. Sontag, and R. Stocker, Logarithmic sensing in Bacillus subtilis aerotaxis, npj Syst. Biol. Appl. 3, 16036 (2017).
- M. Adler, M. Erickstad, E. Gutierrez, and A. Groisman, Studies of bacterial aerotaxis in a microfluidic device, Lab Chip 12, 4835 (2012).
- P. Prakash, Y. Baig, F. J. Peaudecerf, and R. E. Goldstein, Dynamics of an algae–bacteria microcosm: Photosynthesis, chemotaxis, and expulsion in inhomogeneous active matter, Proc. Natl. Acad. Sci. USA 122, e2410225122 (2025).
- B. V. Hokmabad, A. Martínez-Calvo, S. Gonzalez La Corte, and S. S. Datta, Spatial self-organization of confined bacterial suspensions, Proc. Natl. Acad. Sci. USA 122, e2503983122 (2025).
- I. Tuval, L. Cisneros, C. Dombrowski, C. W. Wolgemuth, J. O. Kessler, and R. E. Goldstein, Bacterial swimming and oxygen transport near contact lines, Proc. Natl. Acad. Sci. USA 102, 2277 (2005).
- M. A. Bees, Advances in bioconvection, Annu. Rev. Fluid Mech. 52, 449 (2020).
- C. Dombrowski, L. Cisneros, S. Chatkaew, R. E. Goldstein, and J. O. Kessler, Self-concentration and large-scale coherence in bacterial dynamics, Phys. Rev. Lett. 93, 098103 (2004).
- A. Sokolov, R. E. Goldstein, F. I. Feldchtein, and I. S. Aranson, Enhanced mixing and spatial instability in concentrated bacterial suspensions, Phys. Rev. E 80, 031903 (2009).
- B. Ezhilan, A. A. Pahlavan, and D. Saintillan, Chaotic dynamics and oxygen transport in thin films of aerotactic bacteria, Phys. Fluids 24, 091701 (2012).
- M. Holz and S.-H. Chen, Spatio-temporal structure of migrating chemotactic band of Escherichia coli. I. Traveling band profile, Biophys. J. 26, 243 (1979).
- C. Douarche, A. Buguin, H. Salman, and A. Libchaber, E. coli and oxygen: A motility transition, Phys. Rev. Lett. 102, 198101 (2009).
- M. Eisenbach, A. Tamada, G. Omann, J. Segall, R. Firtel, R. Meili, D. Gutnick, M. Varon, J. W. Lengeler, and F. Murakami, Chemotaxis (World Scientific Publishing Company, Singapore, 2004).
- E. F. Keller and L. A. Segel, Traveling bands of chemotactic bacteria: A theoretical analysis, J. Theor. Biol. 30, 235 (1971).
- I. R. Lapidus and R. Schiller, A model for traveling bands of chemotactic bacteria, Biophys. J. 22, 1 (1978).
- D. Lauffenburger, C. R. Kennedy, and R. Aris, Traveling bands of chemotactic bacteria in the context of population growth, Bull. Math. Biol. 46, 19 (1984).
- M. Schnitzer, S. Block, and H. Berg, Strategies for chemotaxis, in Biology of the Chemotactic Response, edited by J. P. Armitage and J. M. Lackie (Cambridge University Press, Cambridge, 1990), pp. 15–34.
- B. Mazzag, I. Zhulin, and A. Mogilner, Model of bacterial band formation in aerotaxis, Biophys. J. 85, 3558 (2003).
- B. Ezhilan, R. Alonso-Matilla, and D. Saintillan, On the distribution and swim pressure of run-and-tumble particles in confinement, J. Fluid Mech. 781, R4 (2015).
- A. Rebbapragada, M. S. Johnson, G. P. Harding, A. J. Zuccarelli, H. M. Fletcher, I. B. Zhulin, and B. L. Taylor, The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior, Proc. Natl. Acad. Sci. USA 94, 10541 (1997).
- D. Saintillan and M. J. Shelley, Instabilities and pattern formation in active particle suspensions: Kinetic theory and continuum simulations, Phys. Rev. Lett. 100, 178103 (2008).
- G. Subramanian and D. L. Koch, Critical bacterial concentration for the onset of collective swimming, J. Fluid Mech. 632, 359 (2009).
- T. V. Kasyap and D. L. Koch, Chemotaxis driven instability of a confined bacterial suspension, Phys. Rev. Lett. 108, 038101 (2012).
- B. L. Taylor, I. B. Zhulin, and M. S. Johnson, Aerotaxis and other energy-sensing behavior in bacteria, Annu. Rev. Microbiol. 53, 103 (1999).
- 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).
- A. Al-Ani, D. Toms, D. Kondro, J. Thundathil, Y. Yu, and M. Ungrin, Oxygenation in cell culture: Critical parameters for reproducibility are routinely not reported, PLoS One 13, e0204269 (2018).
- I. B. Zhulin, V. A. Bespalov, M. S. Johnson, and B. L. Taylor, Oxygen taxis and proton motive force in Azospirillum brasilense, J. Bacteriol. 178, 5199 (1996).
- K. J. Burns, G. M. Vasil, J. S. Oishi, D. Lecoanet, and B. P. Brown, Dedalus: A flexible framework for numerical simulations with spectral methods, Phys. Rev. Res. 2, 023068 (2020).
- T. Conway, K. A. Krogfelt, and P. S. Cohen, The life of commensal Escherichia coli in the mammalian intestine, EcoSal Plus 1, 10 (2004).
- M. G. Espey, Role of oxygen gradients in shaping redox relationships between the human intestine and its microbiota, Free Radic. Biol. Med. 55, 130 (2013).
- H. C. Berg, E. coli in Motion (Springer, New York, 2004).
- C. Scherber, A. J. Aranyosi, B. Kulemann, S. P. Thayer, M. Toner, O. Iliopoulos, and D. Irimia, Epithelial cell guidance by self-generated EGF gradients, Integr. Biol. 4, 259 (2012).
- E. Donà, J. D. Barry, G. Valentin, C. Quirin, A. Khmelinskii, A. Kunze, S. Durdu, L. R. Newton, A. Fernandez-Minan, W. Huber, et al., Directional tissue migration through a self-generated chemokine gradient, Nature (London) 503, 285 (2013).
- G. Venkiteswaran, S. W. Lewellis, J. Wang, E. Reynolds, C. Nicholson, and H. Knaut, Generation and dynamics of an endogenous, self-generated signaling gradient across a migrating tissue, Cell 155, 674 (2013).
- L. Tweedy, D. A. Knecht, G. M. Mackay, and R. H. Insall, Self-generated chemoattractant gradients: Attractant depletion extends the range and robustness of chemotaxis, PLoS Biol. 14, e1002404 (2016).
- J. Stock, T. Kazmar, F. Schlumm, E. Hannezo, and A. Pauli, A self-generated toddler gradient guides mesodermal cell migration, Sci. Adv. 8, eadd2488 (2022).
- M. C. Uçar, Z. Alsberga, J. Alanko, M. Sixt, and E. Hannezo, Self-generated chemotaxis of mixed cell populations, Proc. Natl. Acad. Sci. USA 122, e2504064122 (2025).
- A. Shellard and R. Mayor, Collective durotaxis along a self-generated stiffness gradient in vivo, Nature (London) 600, 690 (2021).
- A. A. Fragkopoulos, J. Vachier, J. Frey, F.-M. Le Menn, M. G. Mazza, M. Wilczek, D. Zwicker, and O. Bäumchen, Self-generated oxygen gradients control collective aggregation of photosynthetic microbes, J. R. Soc. Interface 18, 20210553 (2021).
- A. Ancel, H. Visser, Y. Handrich, D. Masman, and Y. L. Maho, Energy saving in huddling penguins, Nature (London) 385, 304 (1997).
- A. Ancel, C. Gilbert, N. Poulin, M. Beaulieu, and B. Thierry, New insights into the huddling dynamics of emperor penguins, Anim. Behav. 110, 91 (2015).
- A. V. Zampetaki, B. Liebchen, A. V. Ivlev, and H. Löwen, Collective self-optimization of communicating active particles, Proc. Natl. Acad. Sci. USA 118, e2111142118 (2021).
- D. Ghosh, B. Chakrabarti, and X. Cheng, Source data and simulation code for “Density-controlled reversal of collective migration in bacterial aerotaxis”, Zenodo, 2026, https://doi.org/10.5281/zenodo.20048642.
- W. Niblack, An Introduction to Digital Image Processing (Strandberg Publishing Company, Birkerød, Denmark, 1985).
- L. A. Segel, Incorporation of receptor kinetics into a model for bacterial chemotaxis, J. Theor. Biol. 57, 23 (1976).
- D. Grünbaum, Advection-diffusion equations for internal state-mediated random walks, SIAM J. Appl. Math. 61, 43 (2000).
- B. C. Mazzag, Mathematical Models in Biology (University of California, Davis, 2002).