Magnetic cilia carpets with programmable metachronal waves.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
26 05 2020
26 05 2020
Historique:
received:
03
09
2019
accepted:
27
04
2020
entrez:
28
5
2020
pubmed:
28
5
2020
medline:
25
8
2020
Statut:
epublish
Résumé
Metachronal waves commonly exist in natural cilia carpets. These emergent phenomena, which originate from phase differences between neighbouring self-beating cilia, are essential for biological transport processes including locomotion, liquid pumping, feeding, and cell delivery. However, studies of such complex active systems are limited, particularly from the experimental side. Here we report magnetically actuated, soft, artificial cilia carpets. By stretching and folding onto curved templates, programmable magnetization patterns can be encoded into artificial cilia carpets, which exhibit metachronal waves in dynamic magnetic fields. We have tested both the transport capabilities in a fluid environment and the locomotion capabilities on a solid surface. This robotic system provides a highly customizable experimental platform that not only assists in understanding fundamental rules of natural cilia carpets, but also paves a path to cilia-inspired soft robots for future biomedical applications.
Identifiants
pubmed: 32457457
doi: 10.1038/s41467-020-16458-4
pii: 10.1038/s41467-020-16458-4
pmc: PMC7250860
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2637Références
Golestanian, R., Yeomans, J. M. & Uchida, N. Hydrodynamic synchronization at low Reynolds number. Soft Matter 7, 3074 (2011).
doi: 10.1039/c0sm01121e
Elgeti, J., Winkler, R. G. & Gompper, G. Physics of microswimmers—single particle motion and collective behavior: a review. Rep. Prog. Phys. 78, 056601 (2015).
pubmed: 25919479
doi: 10.1088/0034-4885/78/5/056601
Shapiro, O. H. et al. Vortical ciliary flows actively enhance mass transport in reef corals. Proc. Natl Acad. Sci. USA 111, 13391–13396 (2014).
pubmed: 25192936
doi: 10.1073/pnas.1323094111
Jiménez, B. Restless creatures: the story of life in ten movements. By Matt Wilkinson. New York: Basic Books. $28.99. vii + 308 p.; ill.; index. ISBN: 978-0-465-06572-1 (hc); 978-0-465-09869-9 (eb). 2016. Q. Rev. Biol. 92, 324 (2017).
doi: 10.1086/693606
Osterman, N. & Vilfan, A. Finding the ciliary beating pattern with optimal efficiency. Proc. Natl Acad. Sci. USA 108, 15727–15732 (2011).
pubmed: 21896741
doi: 10.1073/pnas.1107889108
Tilley, A. E., Walters, M. S., Shaykhiev, R. & Crystal, R. G. Cilia dysfunction in lung disease. Annu. Rev. Physiol. 77, 379–406 (2015).
pubmed: 25386990
doi: 10.1146/annurev-physiol-021014-071931
Juan, G. R. R.-S. et al. Multi-scale spatial heterogeneity enhances particle clearance in airway ciliary arrays. Preprint at https://doi.org/10.1101/665125 (2019).
Gilpin, W., Bull, M. S. & Prakash, M. The multiscale physics of cilia and flagella. Nat. Rev. Phys. 2, 74–88 (2020).
doi: 10.1038/s42254-019-0129-0
Nawroth, J. C., van der Does, A. M., Ryan (Firth), A. & Kanso, E. Multiscale mechanics of mucociliary clearance in the lung. Philos. Trans. R. Soc. B Biol. Sci. 375, 20190160 (2020).
doi: 10.1098/rstb.2019.0160
Lyons, R. A., Saridogan, E. & Djahanbakhch, O. The reproductive significance of human fallopian tube cilia. Hum. Reprod. Update 12, 363–372 (2006).
pubmed: 16565155
doi: 10.1093/humupd/dml012
Lauga, E. & Powers, T. R. The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72, 096601 (2009).
doi: 10.1088/0034-4885/72/9/096601
Nyholm, S. V. & McFall-Ngai, M. The winnowing: establishing the squid–vibrio symbiosis. Nat. Rev. Microbiol. 2, 632–642 (2004).
pubmed: 15263898
doi: 10.1038/nrmicro957
Nawroth, J. C. et al. Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome. Proc. Natl Acad. Sci. USA 114, 201706926 (2017).
doi: 10.1073/pnas.1706926114
Gilpin, W., Prakash, V. N. & Prakash, M. Vortex arrays and ciliary tangles underlie the feeding–swimming trade-off in starfish larvae. Nat. Phys. 13, 380–386 (2017).
doi: 10.1038/nphys3981
Ding, Y., Nawroth, J. C., McFall-Ngai, M. J. & Kanso, E. Mixing and transport by ciliary carpets: a numerical study. J. Fluid Mech. 743, 124–140 (2014).
doi: 10.1017/jfm.2014.36
Ding, Y. & Kanso, E. Selective particle capture by asynchronously beating cilia. Phys. Fluids 27, 121902 (2015).
doi: 10.1063/1.4938558
Elgeti, J. & Gompper, G. Emergence of metachronal waves in cilia arrays. Proc. Natl Acad. Sci. USA 110, 4470–4475 (2013).
pubmed: 23487771
doi: 10.1073/pnas.1218869110
Gueron, S. & Levit-Gurevich, K. Energetic considerations of ciliary beating and the advantage of metachronal coordination. Proc. Natl Acad. Sci. USA 96, 12240–12245 (1999).
pubmed: 10535905
doi: 10.1073/pnas.96.22.12240
Polin, M., Tuval, I., Drescher, K., Gollub, J. P. & Goldstein, R. E. Chlamydomonas swims with two “gears” in a eukaryotic version of run-and-tumble locomotion. Science 325, 487–490 (2009).
pubmed: 19628868
doi: 10.1126/science.1172667
Milana, E., Gorissen, B., Peerlinck, S., Volder, M. & Reynaerts, D. Artificial soft cilia with asymmetric beating patterns for biomimetic low‐Reynolds‐number fluid propulsion. Adv. Funct. Mater. 29, 1900462 (2019).
doi: 10.1002/adfm.201900462
van Oosten, C. L., Bastiaansen, C. W. M. & Broer, D. J. Printed artificial cilia from liquid-crystal network actuators modularly driven by light. Nat. Mater. 8, 677–682 (2009).
pubmed: 19561599
doi: 10.1038/nmat2487
Orbay, S., Ozcelik, A., Bachman, H. & Huang, T. J. Acoustic actuation of in situ fabricated artificial cilia. J. Micromech. Microeng. 28, 025012 (2018).
pubmed: 30479458
pmcid: 6251322
doi: 10.1088/1361-6439/aaa0ae
Toonder, J. Den et al. Artificial cilia for active micro-fluidic mixing. Lab Chip 8, 533 (2008).
pubmed: 18369507
doi: 10.1039/b717681c
Vilfan, M. et al. Self-assembled artificial cilia. Proc. Natl Acad. Sci. USA 107, 1844–1847 (2010).
pubmed: 19934055
doi: 10.1073/pnas.0906819106
Khaderi, S. N. et al. Magnetically-actuated artificial cilia for microfluidic propulsion. Lab Chip 11, 2002 (2011).
pubmed: 21331419
doi: 10.1039/c0lc00411a
Hanasoge, S., Hesketh, P. J. & Alexeev, A. Microfluidic pumping using artificial magnetic cilia. Microsyst. Nanoeng. 4, 11 (2018).
pubmed: 31057899
pmcid: 6161502
doi: 10.1038/s41378-018-0010-9
Shields, A. R. et al. Biomimetic cilia arrays generate simultaneous pumping and mixing regimes. Proc. Natl Acad. Sci. USA 107, 15670–15675 (2010).
pubmed: 20798342
doi: 10.1073/pnas.1005127107
den Toonder, J. M. J. & Onck, P. R. Microfluidic manipulation with artificial/bioinspired cilia. Trends Biotechnol. 31, 85–91 (2013).
pubmed: 23245658
doi: 10.1016/j.tibtech.2012.11.005
Hanasoge, S., Hesketh, P. J. & Alexeev, A. Metachronal motion of artificial magnetic cilia. Soft Matter 14, 3689–3693 (2018).
pubmed: 29737998
doi: 10.1039/C8SM00549D
Tsumori, F. et al. Metachronal wave of artificial cilia array actuated by applied magnetic field. Jpn. J. Appl. Phys. 55, 06GP19 (2016).
doi: 10.7567/JJAP.55.06GP19
Kim, J. H. et al. Remote manipulation of droplets on a flexible magnetically responsive film. Sci. Rep. 5, 17843 (2015).
pubmed: 26648418
pmcid: 4673453
doi: 10.1038/srep17843
Zhu, Y., Antao, D. S., Xiao, R. & Wang, E. N. Real-time manipulation with magnetically tunable structures. Adv. Mater. 26, 6442–6446 (2014).
pubmed: 25047631
doi: 10.1002/adma.201401515
Ben, S. et al. Cilia-inspired flexible arrays for intelligent transport of viscoelastic microspheres. Adv. Funct. Mater. 28, 1706666 (2018).
doi: 10.1002/adfm.201706666
Bruot, N. & Cicuta, P. Realizing the physics of motile cilia synchronization with driven colloids. Annu. Rev. Condens. Matter Phys. 7, 323–348 (2015).
doi: 10.1146/annurev-conmatphys-031115-011451
Kotar, J., Leoni, M., Bassetti, B., Lagomarsino, M. C. & Cicuta, P. Hydrodynamic synchronization of colloidal oscillators. Proc. Natl Acad. Sci. USA 107, 7669–7673 (2010).
pubmed: 20385848
doi: 10.1073/pnas.0912455107
Brumley, D. R., Polin, M., Pedley, T. J. & Goldstein, R. E. Hydrodynamic synchronization and metachronal waves on the surface of the colonial alga Volvox carteri. Phys. Rev. Lett. 109, 28–32 (2012).
doi: 10.1103/PhysRevLett.109.268102
Chen, T. & Shea, K. An autonomous programmable actuator and shape reconfigurable structures using bistability and shape memory polymers. 3D Print. Addit. Manuf. 5, 91–101 (2018).
doi: 10.1089/3dp.2017.0118
Lum, G. Z. et al. Shape-programmable magnetic soft matter. Proc. Natl Acad. Sci. USA 113, E6007–E6015 (2016).
pubmed: 27671658
doi: 10.1073/pnas.1608193113
Blake, J. R. & Sleigh, M. A. Mechanics of ciliary locomotion. Biol. Rev. Camb. Philos. Soc. 49, 85–125 (1974).
pubmed: 4206625
doi: 10.1111/j.1469-185X.1974.tb01299.x
Edelmann, J., Petruska, A. J. & Nelson, B. J. Magnetic control of continuum devices. Int. J. Rob. Res. 36, 68–85 (2017).
doi: 10.1177/0278364916683443
Peyron, Q. et al. Kinematic analysis of magnetic continuum robots using continuation method and bifurcation analysis. IEEE Robot. Autom. Lett. 3, 3646–3653 (2018).
doi: 10.1109/LRA.2018.2855803
Petruska, A. J., Edelmann, J. & Nelson, B. J. Model-based calibration for magnetic manipulation. IEEE Trans. Magn. 53, 1–6 (2017).
doi: 10.1109/TMAG.2017.2653080
Purcell, E. M. Life at low Reynolds number. Am. J. Phys. 45, 3–11 (1977).
doi: 10.1119/1.10903
Eloy, C. & Lauga, E. Kinematics of the most efficient cilium. Phys. Rev. Lett. 109, 038101 (2012).
pubmed: 22861901
doi: 10.1103/PhysRevLett.109.038101
Knight-Jones, E. W. Relations between metachronism and the direction of ciliary beat in metazoa. Q. J. Microsc. Sci. 95, 503–521 (1954).
Gu, H., Boehler, Q., Ahmed, D. & Nelson, B. J. Magnetic quadrupole assemblies with arbitrary shapes and magnetizations. Sci. Robot. 4, eaax8977 (2019).
doi: 10.1126/scirobotics.aax8977
Cui, J. et al. Nanomagnetic encoding of shape-morphing micromachines. Nature 575, 164–168 (2019).
pubmed: 31695212
doi: 10.1038/s41586-019-1713-2
Venkiteswaran, V. K., Samaniego, L. F. P., Sikorski, J. & Misra, S. Bio-inspired terrestrial motion of magnetic soft millirobots. IEEE Robot. Autom. Lett. 4, 1753–1759 (2019).
doi: 10.1109/LRA.2019.2898040
Hu, W., Lum, G. Z., Mastrangeli, M. & Sitti, M. Small-scale soft-bodied robot with multimodal locomotion. Nature 554, 81–85 (2018).
pubmed: 29364873
doi: 10.1038/nature25443
Xu, T., Zhang, J., Salehizadeh, M., Onaizah, O. & Diller, E. Millimeter-scale flexible robots with programmable three-dimensional magnetization and motions. Sci. Robot. 4, eaav4494 (2019).
doi: 10.1126/scirobotics.aav4494
Lu, H. et al. A bioinspired multilegged soft millirobot that functions in both dry and wet conditions. Nat. Commun. 9, 3944 (2018).
pubmed: 30258072
pmcid: 6158235
doi: 10.1038/s41467-018-06491-9
Zhang, S., Wang, Y., Lavrijsen, R., Onck, P. R. & den Toonder, J. M. J. Versatile microfluidic flow generated by moulded magnetic artificial cilia. Sens. Actuators B Chem. 263, 614–624 (2018).
doi: 10.1016/j.snb.2018.01.189
Dhooge, A., Govaerts, W. & Kuznetsov, Y. A. MATCONT. ACM Trans. Math. Softw. 29, 141–164 (2003).
doi: 10.1145/779359.779362