Imparting magnetic dipole heterogeneity to internalized iron oxide nanoparticles for microorganism swarm control

  • Paul Seung Soo Kim
  • Aaron Becker
  • Yan Ou
  • Anak Agung Julius
  • Min Jun Kim
Research Paper
Part of the following topical collections:
  1. Nanotechnology in Biorobotic Systems


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.


Tetrahymena pyriformis Iron oxide nanoparticles Magnetotaxis Swarm control Microrobot 



This work was supported by the National Science Foundation under CMMI 1000255, CMMI 1000284, and by ARO W911F-11-1-0490.


  1. 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
  2. Brown ID, Connolly JG, Kerkut G (1981) Galvanotaxic response of Tetrahymena vorax. Comp Biochem Physiol Part C: Comp Pharmacol 69:281–291CrossRefGoogle Scholar
  3. Cheang UK, Roy D, Lee JH, Kim MJ (2010) Fabrication and magnetic control of bacteria-inspired robotic microswimmers. Appl Phys Lett 97: 213704Google Scholar
  4. Dreyfus R, Baudry J, Roper ML, Fermigier M, Stone HA, Bibette J (2005) Microsc Artif Swim. Nature 437:862–865CrossRefGoogle Scholar
  5. Ghosh A, Fischer P (2009) Controlled propulsion of artificial magnetic nanostructured propellers. Nano Lett 9:2243–2245. doi: 10.1021/nl900186w CrossRefGoogle Scholar
  6. Ghosh A, Paria D, Singh HJ, Venugopalan PL, Ghosh A (2012) Dynamical configurations and bistability of helical nanostructures under external torque. Phys Rev E 86:031401CrossRefGoogle Scholar
  7. 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 15:10817–10823CrossRefGoogle Scholar
  8. 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 CrossRefGoogle Scholar
  9. Kim DH, Casale D, Kőhidai L, Kim MJ (2009) Galvanotactic and phototactic control of Tetrahymena pyriformis as a microfluidic workhorse. Appl Phys Lett 94:163901CrossRefGoogle Scholar
  10. 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 97:173702CrossRefGoogle Scholar
  11. 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 8:273–279CrossRefGoogle Scholar
  12. Kim DH, Kim PSS, Agung Julius AA, Kim MJ (2012a) Three-dimensional control of Tetrahymena pyriformis using artificial magnetotaxis. Appl Phys Lett 100: 053702Google Scholar
  13. Kim M, Steager E, Julius AA, Agung J (2012b) Microbiorobotics: biologically inspired microscale robotic systems. William AndrewGoogle Scholar
  14. 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
  15. 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 CrossRefGoogle Scholar
  16. Köhidai L, Csaba G (1998) Chemotaxis and chemotactic selection induced with cytokines (IL-8, Rantes and TNF-α) in the unicellular Tetrahymena pyriformis. Cytokine 10:481–486CrossRefGoogle Scholar
  17. Lavin DP, Hatzis C, Srienc F, Fredrickson A (1990) Size effects on the uptake of particles by populations of Tetrahymena pyriformis cells. J Protozool 37:157–163CrossRefGoogle Scholar
  18. 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: 144101Google Scholar
  19. 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 233904CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. Morozov KI, Leshansky AM (2014) The chiral magnetic nanomotors. Nanoscale 6:1580–1588CrossRefGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. 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 CrossRefGoogle Scholar
  25. 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 Google Scholar
  26. 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
  27. Peyer KE, Zhang L, Nelson BJ (2012b) Bio-inspired magnetic swimming microrobots for biomedical applications. Nanoscale. doi: 10.1039/c2nr32554c Google Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. Zhang L, Peyer KE, Nelson BJ (2010) Artificial bacterial flagella for micromanipulation. Lab Chip 10:2203–2215CrossRefGoogle Scholar
  32. Zhang L, Petit T, Peyer KE, Nelson BJ (2012) Targeted cargo delivery using a rotating nickel nanowire. Nanomedicine: nanotechnology. Biol Med 8:1074–1080Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Paul Seung Soo Kim
    • 1
  • Aaron Becker
    • 2
  • Yan Ou
    • 3
  • Anak Agung Julius
    • 3
  • Min Jun Kim
    • 1
  1. 1.Department of Mechanical Engineering and MechanicsDrexel UniversityPhiladelphiaUSA
  2. 2.Department of Cardiovascular SurgeryHarvard UniversityBostonUSA
  3. 3.Department of Electrical, Computer, and Systems EngineeringRensselaer Polytechnic InstituteTroyUSA

Personalised recommendations