Abstract
Tetrahymena pyriformis is a single cell eukaryote that can be modified to respond to magnetic fields, a response called magnetotaxis. Naturally, this microorganism cannot respond to magnetic fields, but after modification using iron oxide nanoparticles, cells are magnetized and exhibit a constant magnetic dipole strength. In experiments, a rotating field is applied to cells using a two-dimensional approximate Helmholtz coil system. Using rotating magnetic fields, we characterize discrete cells’ swarm swimming which is affected by several factors. The behavior of the cells under these fields is explained in detail. After the field is removed, relatively straight swimming is observed. We also generate increased heterogeneity within a population of cells to improve controllability of a swarm, which is explored in a cell model. By exploiting this straight swimming behavior, we propose a method to control discrete cells utilizing a single global magnetic input. Successful implementation of this swarm control method would enable teams of microrobots to perform a variety of in vitro microscale tasks impossible for single microrobots, such as pushing objects or simultaneous micromanipulation of discrete entities.
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Becker A, Yan O, Kim P, Min Jun K, Julius A Feedback control of many magnetized: Tetrahymena pyriformis cells by exploiting phase inhomogeneity. In: Intelligent Robots and Systems (IROS), 2013 IEEE/RSJ International Conference on, 3–7 Nov. 2013 2013. pp 3317-3323. doi:10.1109/IROS.2013.6696828
Brown ID, Connolly JG, Kerkut G (1981) Galvanotaxic response of Tetrahymena vorax. Comp Biochem Physiol Part C: Comp Pharmacol 69:281–291
Cheang UK, Roy D, Lee JH, Kim MJ (2010) Fabrication and magnetic control of bacteria-inspired robotic microswimmers. Appl Phys Lett 97: 213704
Dreyfus R, Baudry J, Roper ML, Fermigier M, Stone HA, Bibette J (2005) Microsc Artif Swim. Nature 437:862–865
Ghosh A, Fischer P (2009) Controlled propulsion of artificial magnetic nanostructured propellers. Nano Lett 9:2243–2245. doi:10.1021/nl900186w
Ghosh A, Paria D, Singh HJ, Venugopalan PL, Ghosh A (2012) Dynamical configurations and bistability of helical nanostructures under external torque. Phys Rev E 86:031401
Ghosh A, Mandal P, Karmakar S, Ghosh A (2013) Analytical theory and stability analysis of an elongated nanoscale object under external torque. Phys Chem Chem Phys 15:10817–10823
Jo BH, Van Lerberghe LM, Motsegood KM, Beebe DJ (2000) Three-dimensional micro-channel fabrication in polydimethylsiloxane (PDMS) elastomer. J Microelectromech Syst 9:76–81. doi:10.1109/84.825780
Kim DH, Casale D, Kőhidai L, Kim MJ (2009) Galvanotactic and phototactic control of Tetrahymena pyriformis as a microfluidic workhorse. Appl Phys Lett 94:163901
Kim DH, Cheang UK, Kőhidai L, Byun D, Kim MJ (2010) Artificial magnetotactic motion control of Tetrahymena pyriformis using ferromagnetic nanoparticles: a tool for fabrication of microbiorobots. Appl Phys Lett 97:173702
Kim DH, Brigandi SE, Kim P, Byun D, Kim MJ (2011) Characterization of deciliation-regeneration process of tetrahymena pyriformis for cellular robot fabrication. J Bionic Eng 8:273–279
Kim DH, Kim PSS, Agung Julius AA, Kim MJ (2012a) Three-dimensional control of Tetrahymena pyriformis using artificial magnetotaxis. Appl Phys Lett 100: 053702
Kim M, Steager E, Julius AA, Agung J (2012b) Microbiorobotics: biologically inspired microscale robotic systems. William Andrew
Kim PSS, Becker A, Yan O, Julius AA, Min Jun K (2013) Swarm control of cell-based microrobots using a single global magnetic field. In: Ubiquitous Robots and Ambient Intelligence (URAI), 2013. 10th International Conference on, Oct 30 2013–Nov 2 2013. pp 21–26. doi:10.1109/URAI.2013.6677461
Köhidai L, Csaba G (1995) Effects of the mammalian vasoconstrictor the immunocytological detection of endogenous activity. Comp Biochem Physiol C: Pharmacol Toxicol Endocrinol 111:311–316. doi:10.1016/0742-8413(95)00055-S
Köhidai L, Csaba G (1998) Chemotaxis and chemotactic selection induced with cytokines (IL-8, Rantes and TNF-α) in the unicellular Tetrahymena pyriformis. Cytokine 10:481–486
Lavin DP, Hatzis C, Srienc F, Fredrickson A (1990) Size effects on the uptake of particles by populations of Tetrahymena pyriformis cells. J Protozool 37:157–163
Mahoney AW, Nelson ND, Peyer KE, Nelson BJ, Abbott JJ (2014) Behavior of rotating magnetic microrobots above the step-out frequency with application to control of multi-microrobot systems. Appl Phys Lett 104: 144101
Martel S, Tremblay CC, Ngakeng S, Langlois G (2006) Controlled manipulation and actuation of micro-objects with magnetotactic bacteria. Appl Phys Lett 89:233904. doi:10.1063/1.2402221 233904
Martel S et al (2009a) MRI-based medical nanorobotic platform for the control of magnetic nanoparticles and flagellated bacteria for target interventions in human capillaries. Int J Robot Res 28:1169–1182. doi:10.1177/0278364908104855
Martel S, Mohammadi M, Felfoul O, Lu Z, Pouponneau P (2009b) Flagellated magnetotactic bacteria as controlled MRI-trackable propulsion and steering systems for medical nanorobots operating in the human microvasculature. Int J Robot Res 28:571–582. doi:10.1177/0278364908100924
Morozov KI, Leshansky AM (2014) The chiral magnetic nanomotors. Nanoscale 6:1580–1588
Nam S-W, Van Noort D, Yang Y, Park S (2007) A biological sensor platform using a pneumatic-valve controlled microfluidic device containing Tetrahymena pyriformis. Lab Chip 7:638–640. doi:10.1039/b617357h
Ogawa N, Oku H, Hashimoto K, Ishikawa M (2006) A physical model for galvanotaxis of Paramecium cell. J Theor Biol 242:314–328. doi:10.1016/j.jtbi.2006.02.021
Ou Y, Kim DH, Kim P, Kim MJ, Julius AA (2012) Motion control of magnetized Tetrahymena pyriformis cells by magnetic field with Model Predictive Control. Int J Robot Res. doi:10.1177/0278364912464669
Peyer KE, Tottori S, Qiu F, Zhang L, Nelson BJ (2012a) Magnetic helical micromachines. Chem A Eur J 19: 28–38. doi:10.1002/chem.201203364
Peyer KE, Zhang L, Nelson BJ (2012b) Bio-inspired magnetic swimming microrobots for biomedical applications. Nanoscale. doi:10.1039/c2nr32554c
Tottori S, Zhang L, Qiu F, Krawczyk KK, Franco-Obregón A, Nelson BJ (2012) Magnetic helical micromachines: fabrication, controlled swimming, and cargo transport. Adv Mater 24:811–816. doi:10.1002/adma.201103818
Weibel DB, Garstecki P, Ryan D, DiLuzio WR, Mayer M, Seto JE, Whitesides GM (2005) Microoxen: microorganisms to move microscale loads. Proc Natl Acad Sci USA 102:11963–11967. doi:10.1073/pnas.0505481102
Zhang L, Abbott JJ, Dong L, Kratochvil BE, Bell D, Nelson BJ (2009) Artificial bacterial flagella: fabrication and magnetic control. Appl Phys Lett 94:064107. doi:10.1063/1.3079655
Zhang L, Peyer KE, Nelson BJ (2010) Artificial bacterial flagella for micromanipulation. Lab Chip 10:2203–2215
Zhang L, Petit T, Peyer KE, Nelson BJ (2012) Targeted cargo delivery using a rotating nickel nanowire. Nanomedicine: nanotechnology. Biol Med 8:1074–1080
Acknowledgments
This work was supported by the National Science Foundation under CMMI 1000255, CMMI 1000284, and by ARO W911F-11-1-0490.
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Guest Editors: Leonardo Ricotti, Arianna Menciassi
This article is part of the topical collection on Nanotechnology in Biorobotic Systems
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Kim, P.S.S., Becker, A., Ou, Y. et al. Imparting magnetic dipole heterogeneity to internalized iron oxide nanoparticles for microorganism swarm control. J Nanopart Res 17, 144 (2015). https://doi.org/10.1007/s11051-014-2746-y
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DOI: https://doi.org/10.1007/s11051-014-2746-y