- Physical Review Journals
All JournalsPhysics Magazine

PRX Life

Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Open Access

Physical Confinement Regulates Transitions in Nematode Motility

M Sreepadmanabh1,*, Saheli Dey1,2,*, Sayan Kundu1,3, Ashitha B. Arun1, Sandhya P. Koushika4, Shashi Thutupalli1,5,6, Duncan Hewitt7, and Tapomoy Bhattacharjee1,†

  • *These authors contributed equally to this work.
  • †Contact author: tapa@ncbs.res.in
PDF

PRX Life 3, 043014 – Published 24 November, 2025

DOI: https://doi.org/10.1103/sdhy-5g9n

Abstract

How do worms navigate their complex natural surroundings? Laboratory studies using nematodes such as Caenorhabditis elegans interrogate motility patterns as an indicator of their behavioral responses using liquid cultures or two-dimensional (2D) agar pads. However, C. elegans typically inhabit three-dimensional granular niches—such as soft soil and decomposed biological matter—with spatiotemporally varying viscoelastoplastic material properties that impose physical constraints on their motion. Here, by directly visualizing worm motility in transparent 3D granular matrices with tunable mechanical properties, we find that the propulsive speed of nematodes shows a nonmonotonic dependence on the yield stress of their microenvironment. Biophysical measurements reveal that this nonmonotonicity emerges as nematodes optimize for efficient navigation under higher confinement by matching their forward propulsive speed to the wave speed along their body. This regulation of locomotory behavior is purely dictated by the physical interaction of the nematode with its environment without involving soft-touch sensory neurons. Remarkably, our predictions from a slender body theory of undulatory motion in yield stress environments exactly capture the scaling behavior for both efficiency and mode of motion as obtained from the experimental data. Further, in a nondimensionalized phase space defined by propulsive efficiency and timescale of motility, we show that increasing confinement leads to a sharp gait transition from poorly efficient thrashing to highly efficient crawling. Our work thus establishes a biophysical paradigm wherein the physical interaction of worms with their mechanical microenvironment leads to a transition between distinct modes of undulatory motion, entirely as a consequence of 3D physical confinement.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (39)

  1. M.-A. Félix and C. Braendle, The natural history of Caenorhabditis elegans, Curr. Biol. 20, R965 (2010).
  2. H. Schulenburg and M. A. Félix, The natural biotic environment of caenorhabditis elegans, Genetics 206, 55 (2017).
  3. Y. Xu et al., Dopamine receptor DOP-1 engages a sleep pathway to modulate swimming in C. elegans, iScience 24, 102247 (2021).
  4. A. Vidal-Gadea et al., Caenorhabditis elegans selects distinct crawling and swimming gaits via dopamine and serotonin, Proc. Natl. Acad. Sci. USA 108, 17504 (2011).
  5. R. Ghosh and S. W. Emmons, Episodic swimming behavior in the nematode C. elegans, J. Exp. Biol. 211, 3703 (2008).
  6. R. Laranjeiro, G. Harinath, D. Burke, B. P. Braeckman, and M. Driscoll, Single swim sessions in C. elegans induce key features of mammalian exercise, BMC Biol. 15, 30 (2017).
  7. J. T. Pierce-Shimomura et al., Genetic analysis of crawling and swimming locomotory patterns in C. elegans, Proc. Natl. Acad. Sci. USA 105, 20982 (2008).
  8. F. Lebois et al., Locomotion control of caenorhabditis elegans through confinement, Biophys. J. 102, 2791 (2012).
  9. J. Korta, D. A. Clark, C. V. Gabel, L. Mahadevan, and A. D. T. Samuel, Mechanosensation and mechanical load modulate the locomotory gait of swimming C. elegans, J. Exp. Biol. 210, 2383 (2007).
  10. C. Beron et al., The burrowing behavior of the nematode Caenorhabditis elegans: A new assay for the study of neuromuscular disorders, Genes Brain Behav. 14, 357 (2015).
  11. X. N. Shen and P. E. Arratia, Undulatory swimming in viscoelastic fluids, Phys. Rev. Lett. 106, 208101 (2011).
  12. D. A. Gagnon, X. N. Shen, and P. E. Arratia, Undulatory swimming in fluids with polymer networks, Europhys. Lett. 104, 14004 (2013).
  13. J. Sznitman and P. E. Arratia, Locomotion through complex fluids: An experimental view, in Complex Fluids in Biological Systems: Experiment, Theory, and Computation, Biological and Medical Physics, Biomedical Engineering, edited by S. Spagnolie (Springer, New Y, 2015), pp. 245–281.
  14. S. Park et al., Enhanced caenorhabditis elegans locomotion in a structured microfluidic environment, PLoS One 3, e2550 (2008).
  15. D. A. Gagnon and P. E. Arratia, The cost of swimming in generalized Newtonian fluids: Experiments with C. elegans, J. Fluid Mech. 800, 753 (2016).
  16. J. Sznitman, X. Shen, P. K. Purohit, and P. E. Arratia, The effects of fluid viscosity on the kinematics and material properties of C. elegans swimming at low Reynolds number, Proc. Soc. Exp. Mech. 50, 1303 (2010).
  17. J. Sznitman, P. K. Purohit, P. Krajacic, T. Lamitina, and P. E. Arratia, Material properties of caenorhabditis elegans swimming at low Reynolds number, Biophys. J. 98, 617 (2010).
  18. J. S. Park, D. Kim, J. H. Shin, and D. A. Weitz, Efficient nematode swimming in a shear thinning colloidal suspension, Soft Matter 12, 1892 (2016).
  19. A. Guisnet, M. Maitra, S. Pradhan, and M. Hendricks, A three-dimensional habitat for C. elegans environmental enrichment, PLoS One 16, e0245139 (2021).
  20. M. Tahernia, M. Mohammadifar, and S. Choi, Paper-supported high-throughput 3D culturing, trapping, and monitoring of Caenorhabditis elegans, Micromachines (Basel) 11, 99 (2020).
  21. S. Jung, Caenorhabditis elegans swimming in a saturated particulate system, Phys. Fluids 22, 031903 (2010).
  22. G. Juarez, K. Lu, J. Sznitman, and P. E. Arratia, Motility of small nematodes in wet granular media, Europhys. Lett. 92, 44002 (2010).
  23. M. Sreepadmanabh, A. B. Arun, and T. Bhattacharjee, Design approaches for 3D cell culture and 3D bioprinting platforms, Biophys. Rev. 5, 021304 (2024).
  24. T. Bhattacharjee et al., Liquid-like solids support cells in 3D, ACS Biomater. Sci. Eng. 2, 1787 (2016).
  25. T. Bhattacharjee et al., Polyelectrolyte scaling laws for microgel yielding near jamming, Soft Matter 14, 1559 (2018).
  26. See Supplemental Material at http://link.aps.org/supplemental/10.1103/sdhy-5g9n for additional figures and details of the theoretical formulation, which also contains Ref. [28].
  27. R. O'Hagan, M. Chalfie, and M. B. Goodman, The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals, Nat. Neurosci. 8, 43 (2004).
  28. D. R. Hewitt and N. J. Balmforth, Locomotion with a wavy cylindrical filament in a yield-stress fluid, J. Fluid Mech. 936, A17 (2022).
  29. D. R. Hewitt, Swimming in viscoplastic fluids, Rheol. Acta 63, 673 (2024).
  30. C. Fang-Yen et al., Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans, Proc. Natl. Acad. Sci. USA 107, 20323 (2010).
  31. A. Kudrolli and B. Ramirez, Burrowing dynamics of aquatic worms in soft sediments, Proc. Natl. Acad. Sci. USA 116, 25569 (2019).
  32. K. M. Dorgan, C. J. Law, and G. W. Rouse, Meandering worms: Mechanics of undulatory burrowing in muds, Proc. R. Soc. B. Biol. Sci. 280, (2013).
  33. P. E. Arratia, Life in complex fluids: Swimming in polymers, Phys. Rev. Fluids 7, 110515 (2022).
  34. M. Sreepadmanabh, M. Ganesh, R. Bhat, and T. Bhattacharjee, Jammed microgel growth medium prepared by flash-solidification of agarose for 3D cell culture and 3D bioprinting, Biomed. Mater. 18, 045011 (2023).
  35. T. Ahamed, A. C. Costa, and G. J. Stephens, Capturing the continuous complexity of behaviour in Caenorhabditis elegans, Nat. Phys. 17, 275 (2020).
  36. E. D. Tytell, P. Holmes, and A. H. Cohen, Spikes alone do not behavior make: Why neuroscience needs biomechanics, Curr. Opin. Neurobiol. 21, 816 (2011).
  37. A. Bilbao, A. K. Patel, M. Rahman, S. A. Vanapalli, and J. Blawzdziewicz, Roll maneuvers are essential for active reorientation of Caenorhabditis elegans in 3D media, Proc. Natl. Acad. Sci. USA 115, E3616 (2018).
  38. M. Sreepadmanabh et al., Cell shape affects bacterial colony growth under physical confinement, Nat. Commun. 15, 9561 (2024).
  39. T. Bhattacharjee and S. S. Datta, Bacterial hopping and trapping in porous media, Nat. Commun. 10, 2075 (2019).

Outline

Information

PRX Life 3, 043014– Published 24 November, 2025
  • Received 6 April 2025
  • Accepted 27 October 2025
Crossmark - Check for updates button
Creative Commons Logo

Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

Published by the American Physical Society

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation