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Enhanced Caenorhabditis elegans Locomotion in a Structured Microfluidic Environment
Open accessAbstract
BACKGROUND: Behavioral studies of Caenorhabditis elegans traditionally are done on the smooth surface of agar plates, but the natural habitat of C. elegans and other nematodes is the soil, a complex and structured environment. In order to investigate how worms move in such environments, we have developed a technique to study C. elegans locomotion in microstructures fabricated from agar. METHODOLOGY/PRINCIPAL FINDINGS: When placed in open, liquid-filled, microfluidic chambers containing a square array of posts, we discovered that worms are capable of a novel mode of locomotion, which combines the fast gait of swimming with the more efficient movements of crawling. When the wavelength of the worms matched the periodicity of the post array, the microstructure directed the swimming and increased the speed of C. elegans ten-fold. We found that mutants defective in mechanosensation (mec-4, mec-10) or mutants with abnormal waveforms (unc-29) did not perform this enhanced locomotion and moved much more slowly than wild-type worms in the microstructure. CONCLUSION/SIGNIFICANCE: These results show that the microstructure can be used as a behavioral screen for mechanosensory and uncoordinated mutants. It is likely that worms use mechanosensation in the movement and navigation through heterogeneous environments.
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“In particular, arrays of microfluidic posts (“artificial dirt”) have recently been developed specifically for this purpose (Lockery et al., 2008; Park et al., 2008).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Park et al., 2008
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“We find that the model copes well with these environments, producing remarkably realistic locomotion when compared to the reported behavior (Lockery et al., 2008; Park et al., 2008).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Park et al., 2008
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“Specifically, as in the experiments, the model yields crawling behavior in the hexagonal post configuration (Movies S3–S5 in Supplementary Material; Lockery et al., 2008) and swimming like motion in the cubic configuration (Movie S6 in Supplementary Material; Park et al., 2008).”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Park et al., 2008
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Borne, F., Kasimatis, K. R., & Phillips, P. C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0189679 · Cited by 19
“The chambers all have a 156 pillar-array to facilitate the natural, sinusoidal movement of worms [35,36].”
BackgroundMicrofluidics for mechanobiology of model organisms
Kim, A. A., Nekimken, A. L., Fechner, S., O’Brien, L. E., & Pruitt, B. L. (2018) · Methods in cell biology · doi:10.1016/bs.mcb.2018.05.010 · Cited by 22
“…of worm locomotion in microfluidic chambers that focus on characterizing crawling and swimming in different environments (Lockery et al., 2008), this paper dissected mechanobiological pathways by showing the effect of knocking out genes that are essential for mechanosensation (Park et al., 2008).”
BackgroundMethodInfluentialStress response ofCaenorhabditis elegansinduced by space crowding in a micro-column array chip
Wang, X., Tang, L., Xia, Y., Hu, L., Feng, X., Du, W., & Liu, B. (2013) · Integrative Biology · doi:10.1039/c3ib20289e · Cited by 18
Dynamics of scattering in undulatory active collisions
Rieser, J. M., Schiebel, P., Pazouki, A., Qian, F., Goddard, Z. C., Wiesenfeld, K. A., Zangwill, A., Negruţ, D., & Goldman, D. I. (2019) · Physical review. E · doi:10.1103/physreve.99.022606 · Cited by 19
Predicting path from undulations forC. elegansusing linear and nonlinear resistive force theory
Keaveny, E. E., & Brown, A. E. (2017) · Physical Biology · doi:10.1088/1478-3975/aa5ce6 · Cited by 17
Puchalt, J. C., Gonzalez-Rojo, J. F., Gómez-Escribano, A. P., Vázquez‐Manrique, R. P., & Sánchez-Salmerón, A.-J. (2022) · Scientific Reports · doi:10.1038/s41598-022-05823-6 · Cited by 16
Walking is like slithering: A unifying, data-driven view of locomotion
Zhao, D., Bittner, B., Clifton, G. T., Gravish, N., & Revzen, S. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2113222119 · Cited by 15
“For example, walking insects (2–4), crawling worms (5, 6), slithering reptiles (7–9), and swimming microorganisms (10, 11) all exhibit such relationships.”
BackgroundYaqoob, B., Rodella, A., Dottore, E. D., Mondini, A., Mazzolai, B., & Pugno, N. M. (2023) · Journal of The Royal Society Interface · doi:10.1098/rsif.2022.0875 · Cited by 12
“During swimming in water, the body’s waveform characteristics differ significantly from crawling on harder media, like agar, in terms of amplitude, wavelength and speed [18,22,42,43].”
BackgroundEscape dynamics of confined undulating worms
Biswas, A., & Kudrolli, A. A. (2023) · Soft Matter · doi:10.1039/d3sm00211j · Cited by 12
Kamal, A., & Keaveny, E. E. (2018) · Journal of The Royal Society Interface · doi:10.1098/rsif.2018.0592 · Cited by 12
“In fluidic environments consisting of posts arranged in a square arrays, or in wet granular media, both experiments [26, 27, 28] and simulations [28, 29] demonstrate enhanced locomotion with speeds of up to ten times the free swimming value when an undulatory swimmer is able to push and pull against the posts or grain…”
Karengera, A., Bao, C., Riksen, J. A. G., van Veelen, H. P. J., Sterken, M. G., Kammenga, J. E., Murk, A. J., & Dinkla, I. J. T. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.112923 · Cited by 11
Haspel, G., Deng, L., Alfonso, M. B. H., & Tanvir, Z. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-816477-8.00001-6 · Cited by 10
On-Demand Isolation and Manipulation of C. elegans by In Vitro Maskless Photopatterning
Oliver, C. R., Gourgou, E., Bazopoulou, D., Chronis, N., & Hart, A. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0145935 · Cited by 11
A microfluidic diode for sorting and immobilization of Caenorhabditis elegans
Yang, L., Hong, T., Zhang, Y., Arriola, J. G. S., Nelms, B. L., Mu, R. R., & Li, D. (2017) · Biomedical Microdevices · doi:10.1007/s10544-017-0175-2 · Cited by 10
Sterling, P., & Laughlin, S. B. (2023) · Animal Cognition · doi:10.1007/s10071-023-01825-7 · Cited by 11
Caenorhabditis Elegans Segmentation Using Texture-Based Models for Motility Phenotyping
Greenblum, A., Sznitman, R., Fua, P., Arratia, P. E., & Sznitman, J. (2014) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2014.2298612 · Cited by 9
Doh, J. H., Moore, A. B., Çelen, İ., Moore, M. T., & Sabanayagam, C. R. (2016) · Journal of Biological Methods · doi:10.14440/jbm.2016.109 · Cited by 10
Miniaturized Sensors and Actuators for Biological Studies on Small Model Organisms of Disease
Youssef, K., Bayat, P., Peimani, A. R., Dibaji, S., & Rezai, P. (2017) · Energy, environment, and sustainability · doi:10.1007/978-981-10-7751-7_9 · Cited by 11
Aceves-Sánchez, P., Degond, P., Keaveny, E. E., Manhart, A., Merino-Aceituno, S., & Peurichard, D. (2020) · Bulletin of Mathematical Biology · doi:10.1007/s11538-020-00805-z · Cited by 10
Analysis of Freely Swimming C. elegans Using Laser Diffraction
Magnes, J., Raley‐Susman, K. M., Melikechi, N., Sampson, A., Eells, R., Bello, A., & Lueckheide, M. J. (2012) · Open Journal of Biophysics · doi:10.4236/ojbiphy.2012.23013 · Cited by 10
“The worms navigate the environment with novel locomotory patterns, so-called “enhanced swimming” that relies on mechanosensory neuron signal transduction [7].”
BackgroundNam, S.-W., Qian, C., Kim, S. H., van Noort, D., Chiam, K., & Park, S. (2013) · Scientific Reports · doi:10.1038/srep03247 · Cited by 10
Self-citationAdvanced Microfluidic Assays for Caenorhabditis elegans
Bakhtina, N. A., MacKinnon, N., & Korvink, J. G. (2016) · InTech eBooks · doi:10.5772/64283 · Cited by 10
“To further study crawling behavior, a number of PDMS microfluidic devices were presented that consisted of sinusoidal channels of varying wave‐ lengths [84, 86, 87].”
Optimal Fungal Space Searching Algorithms
Asenova, E., Lin, H., Fu, E., Nicolau, D. V., & Nicolau, D. V. (2016) · IEEE Transactions on NanoBioscience · doi:10.1109/tnb.2016.2567098 · Cited by 9
Metadata
- Authors
- Park, S., Hwang, H., Nam, S.-W., Martinez, F., Austin, R. H., & Ryu, W. S.
- Affiliations
- Ewha Womans University (KR)
- Princeton University (US)
- Corresponding author
- Ryu, William S.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-06-25
- Volume
- 3
- Issue
- 6
- Pages
- e2550
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2430527
- OpenAlex
- W1980172171
- Cited by
- 157
- References
- 18
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 6 · 2023: 10 · 2022: 10 · 2021: 8 · 2020: 8 · 2019: 4 · 2018: 7 · 2017: 7 · 2016: 9 · 2015: 12 · 2014: 8 · 2013: 13 · 2012: 15
- FWCI
- 3.94
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Korea Science and Engineering Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Physical Sciences › Physics and Astronomy › Condensed Matter Physics › Micro and Nano Robotics
- Keywords
- Caenorhabditis elegans, locomotion, swimming, crawling, mechanosensing, mec-4, mec-10, soil environment
- MeSH terms
- Animals, Locomotion, Caenorhabditis elegans, Microfluidics
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