Construction of a microrobot system using magnetotactic bacteria for the separation of Staphylococcus aureus

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Magnetotactic bacteria exhibit superiority over other bacteria in fabricating microrobots because of their high motility and convenient controllability. In this study, a microrobot system is constructed using magnetotactic bacteria MO-1 and applied in pathogenic separation. The feasibility of this approach is demonstrated using Staphylococcus aureus. The MO-1 magnetotactic bacterial microrobots are fabricated by binding magnetotactic bacteria MO-1 with their rabbit anti-MO-1 polyclonal antibodies. The efficient binding of MO-1 magnetotactic bacterial microrobots to Staphylococcus aureus is corroborated by phase contrast microscopic and transmission electron microscopic analyses. Further, a microfluidic chip is designed and produced, and the MO-1 microrobots are magnetically guided toward a sample pool in the chip. In the sample pool, Staphylococcus aureus samples are loaded on the microrobots and then carried away to a detection pool in the chip, suggesting the microrobots have successfully carried and separated pathogen. This study is the first to demonstrate bacterial microrobots carrying pathogens and more importantly, it reflects the great potential of using magnetotactic bacteria to develop magnetic-guided, auto-propelled microrobots for pathogen isolation.

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  1. R. Afshar, Y. Moser, T. Lehnert, M.A. Gijs, Three-dimensional magnetic focusing of superparamagnetic beads for on-chip agglutination assays. Anal. Chem. 83(3), 1022–1029 (2011)

  2. D. Akin, J. Sturgis, K. Ragheb, D. Sherman, K. Burkholder, J.P. Robinson, A.K. Bhunia, S. Mohammed, R. Bashir, Bacteria-mediated delivery of nanoparticles and cargo into cells. Nat. Nanotechnol. 2(7), 441–449 (2007)

  3. D.A. Bazylinski, R.B. Frankel, Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2(3), 217–230 (2004)

  4. B. Behkam, M. Sitti, Bacterial flagella-based propulsion and on/off motion control of microscale objects. Appl. Phys. Lett. 90(2), 023902 (2007)

  5. R.P. Blakemore, Magnetotactic bacteria. Ann. Rev. Microbiol. 36, 217–238 (1982)

  6. U.K. Cheang, D. Roy, J.H. Lee, M.J. Kim, Fabrication and magnetic control of bacteria-inspired robotic microswimmers. Appl. Phys. Lett. 97(21), 213704 (2010)

  7. S. Cho, S.J. Park, S.Y. Ko, J.O. Park, S. Park, Development of bacteria-based microrobot using biocompatible poly (ethylene glycol). Biomed. Microdevices 14(6), 1019–1025 (2012)

  8. N. Darnton, L. Turner, K. Breuer, H.C. Berg, Moving fluid with bacterial carpets. Biophys. J. 86(3), 1863–1870 (2004)

  9. E.F. Delong, R.B. Frankel, D.A. Bazylinski, Multiple evolutionary origins of magnetotaxis in bacteria. Science 259(5096), 803–806 (1993)

  10. R.C. Denomme, Z. Lu, S. Martel, A microsensor for the detection of a single pathogenic bacterium using magnetotactic bacteria-based bio-carriers: Simulations and preliminary experiments. in Proceedings of the 29th Annual International Conference of the IEEE EMBS Cité Internationale, Lyon, France, August 23–26, pp.99 (2007).

  11. J.J. Diao, D. Hua, J. Lin, H.H. Teng, D. Chen, Nanoparticle delivery by controlled bacteria. J. Nanosci. Nanotechnol. 5(10), 1749–1751 (2005)

  12. M. Erntell, U. Sjobring, E.B. Myhre, G. Kronvall, Non-immune fab- and fc- mediated interactions of avian ig with s. Aureus and group c and g streptococci. APMIS 96(3), 239–249 (1988)

  13. R. Fernandes, M. Zuniga, F.R. Sassine, M. Karakoy, D.H. Gracias, Enabling cargo-carrying bacteria via surface attachment and triggered release. Small 7(5), 588–592 (2011)

  14. G.S. Fiorini, D.T. Chiu, Disposable microfluidic devices: fabrication, function, and application. BioTechniques 38(3), 429–446 (2005)

  15. C.B. Flies, J. Peplies, D. Schüler, Combined approach for characterization of uncultivated magnetotactic bacteria from various aquatic environments. Appl. Environ. Microbiol. 71(5), 2723–2731 (2005)

  16. R.B. Frankel, The discovery of magnetotactic/magnetosensitive bacteria. Chin. J. Oceanol. Limn. 27(1), 1–2 (2009)

  17. R.B. Frankel, D.A. Bazylinski, Magnetosomes and magneto-aerotaxis. Contrib. Microbiol. 16, 182–193 (2009)

  18. D.R. Frutiger, K. Vollmers, B.E. Kratochvil, B.J. Nelson, Small, fast, and under control: wireless resonant magnetic micro-agents. Int. J. Robot. Res. 29(5), 613–636 (2009)

  19. J.A. Hennekinne, A. Ostyn, F. Guillier, S. Herbin, A.L. Prufer, S. Dragacci, How should staphylococcal food poisoning outbreaks be characterized? Toxins 2(8), 2106–2116 (2010)

  20. D.A. Kanayeva, R. Wang, D. Rhoads, G.F. Erf, M.F. Slavik, S. Tung, Y. Li, Efficient separation and sensitive detection of listeria monocytogenes using an impedance immunosensor based on magnetic nanoparticles, a microfluidic chip, and an interdigitated microelectrode. J. Food Prot. 75(11), 1951–1959 (2012)

  21. M.G. Kaye, M.J. Fox, J.G. Bartlett, S.S. Braman, J. Glassroth, The clinical spectrum of staphylococcus aureus pulmonary infection. Chest 97(4), 788–792 (1990)

  22. D. Kim, A. Liu, E. Diller, M. Sitti, Chemotactic steering of bacteria propelled microbeads. Biomed. Microdevices 14(6), 1009–1017 (2012)

  23. T. Krell, J. Lacal, F. Munoz-Martinez, J.A. Reyes-Darias, B.H. Cadirci, C. Garcia-Fontana, J.L. Ramos, Diversity at its best: bacterial taxis. Environ. Microbiol. 13(5), 1115–1124 (2011)

  24. C.T. Lefèvre, A. Bernadac, K.Y. Zhang, N. Pradel, L.F. Wu, Isolation and characterization of a magnetotactic bacterial culture from the mediterranean sea. Environ. Microbiol. 11(7), 1646–1657 (2009a)

  25. C.T. Lefèvre, T. Song, J.P. Yonnet, L.F. Wu, Characterization of bacterial magnetotactic behaviors by using a magneto spectrophotometry assay. Appl. Environ. Microbiol. 75(12), 3835–3841 (2009b)

  26. C.T. Lefèvre, N. Menguy, F. Abreu, U. Lins, M. Posfai, T. Prozorov, D. Pignol, R.B. Frankel, D.A. Bazylinski, A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science 334(6063), 1720–1723 (2011)

  27. L.A. Liébana, S. Campoy, J. Barbé, S. Alegret, M. Pividori, Magneto immunoseparation of pathogenic bacteria and electrochemical magneto genosensing of the double-tagged amplicon. Anal. Chem. 81(14), 5812–5820 (2009)

  28. Z. Lu, R. Denomme, S. Martel, Toward bacteria detection on chip: a biosensor based on magnetotactic bacteria and impedance spectroscopy. The 11th International Conference on Miniaturized Systems for Chemistry and Life Sciences (μTAS), Paris, France, October 7–11 (2007a).

  29. Z. Lu, J. El-Fouladi, Y. Savaria, S. Martel, A hybrid bacteria and microparticle detection platform on a CMOS chip. The 11th International Conference on Miniaturized Systems for Chemistry and Life Sciences (μTAS), Paris, France, October 7–11 (2007b).

  30. Q. Ma, C. Chen, S. Wei, C. Chen, L.F. Wu, T. Song, Construction and operation of a microrobot based on magnetotactic bacteria in a microfluidic chip. Biomicrofluidics 6(2), 2410701–2410712 (2012)

  31. V. Magdanz, S. Sanchez, O.G. Schmidt, Development of a sperm-flagella driven micro-bio-robot. Adv. Mater. 25(45), 6581–6588 (2013)

  32. S. Martel, Bacterial microsystems and microrobots. Biomed. Microdevices 14(6), 1033–1045 (2012)

  33. S. Martel, C.C. Tremblay, S. Ngakeng, G. Langlois, Controlled manipulation and actuation of micro-objects with magnetotactic bacteria. Appl. Phys. Lett. 89(23), 233904 (2006)

  34. S. Martel, O. Felfoul, J.B. Mathieu, A. Chanu, S. Tamaz, M. Mohammadi, M. Mankiewicz, N. Tabatabaei, 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(9), 1169–1182 (2009a)

  35. S. Martel, M. Mohammadi, O. Felfoul, Z. Lu, P. Pouponneau, Flagellated magnetotactic bacteria as controlled mri-trackable propulsion and steering systems for medical nanorobots operating in the human microvasculature. Int. J. Robot. Res. 28(4), 571–582 (2009b)

  36. S.J. Park, H. Bae, S.Y. Ko, J.J. Min, J.O. Park, S. Park, Selective bacterial patterning using the submerged properties of micro beads on agarose gel. Biomed. Microdevices 15(5), 793–799 (2013a)

  37. S.J. Park, S.H. Park, S. Cho, D.M. Kim, Y. Lee, S.Y. Ko, Y. Hong, H.E. Choy, J.J. Min, J.O. Park, S. Park, New paradigm for tumor theranostic methodology using bacteria-based microrobot. Sci. Rep. 3, 3394 (2013b)

  38. C. Pawashe, S. Floyd, M. Sitti, Modeling and experimental characterization of an untethered magnetic micro-robot. Int. J. Robot. Res. 28(8), 1077–1094 (2009)

  39. N.P. Pera, A. Kouki, S. Haataja, H.M. Branderhorst, R.M. Liskamp, G.M. Visser, J. Finne, R.J. Pieters, Detection of pathogenic streptococcus suis bacteria using magnetic glycoparticles. Org. Biomol. Chem. 8(10), 2425–2429 (2010)

  40. J. Qiu, Y. Zhou, H. Chen, J.M. Lin, Immunomagnetic separation and rapid detection of bacteria using bioluminescence and microfluidics. Talanta 79(3), 787–795 (2009)

  41. D.D. Richman, P.H. Cleveland, M.N. Oxman, K.M. Johnson, The binding of staphylococcal protein a by the sera of different animal species. J. Immunol. 128(5), 2300–2305 (1982)

  42. R. Schirhagl, E.W. Hall, I. Fuereder, R.N. Zare, Separation of bacteria with imprinted polymeric films. Analyst 137(6), 1495–1499 (2012)

  43. S.L. Simmons, D.A. Bazylinski, K.J. Edwards, South-seeking magnetotactic bacteria in the northern hemisphere. Science 311(5759), 371–374 (2006)

  44. E. Steager, C.B. Kim, J. Patel, S. Bith, C. Naik, L. Reber, M.J. Kim, Control of microfabricated structures powered by flagellated bacteria using phototaxis. Appl. Phys. Lett. 90(26), 263901 (2007)

  45. Y.J. Sung, H.J. Suk, H.Y. Sung, T. Li, H. Poo, M.G. Kim, Novel antibody/gold nanoparticle/magnetic nanoparticle nanocomposites for immunomagnetic separation and rapid colorimetric detection of Staphylococcus aureus in milk. Biosens. Bioelectron. 43, 432–439 (2013)

  46. R.E. Taylor, K. Kim, N. Sun, S.J. Park, J.Y. Sim, G. Fajardo, D. Bernstein, J.C. Wu, B.L. Pruitt, Sacrificial layer technique for axial force post assay of immature cardiomyocytes. Biomed. Microdevices 15(1), 171–181 (2013)

  47. S. Tung, A. Malshea, C.C. Leea, R. Pooran, in Proceeding of the 12th International Conference on Solid state sensors, actuators and microsystems (Transducers ‘03), IEEE, Boston, MA, June 8–12, pp.678 (2003).

  48. J. Verbarg, W.D. Plath, L.C. Shriver-Lake, P.B. Howell, J.S. Erickson, J.P. Golden, F.S. Ligler, Catch and release: Integrated system for multiplexed detection of bacteria. Anal. Chem. 85(10), 4944–4950 (2013)

  49. W.J. Zhang, C.L. Santini, A. Bernadac, J. Ruan, S.D. Zhang, T. Kato, Y. Li, K. Namba, L.F. Wu, Complex spatial organization and flagellin composition of flagellar propeller from marine magnetotactic ovoid strain mo-1. J. Mol. Biol. 416(4), 558–570 (2012)

  50. L. Zhao, D. Wu, L.F. Wu, T. Song, A simple and accurate method for quantification of magnetosomes in magnetotactic bacteria by common spectrophotometer. J. Biochem. Biophys. Methods 70(3), 377–383 (2007)

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This work was supported by the State Key Program of National Natural Science of China (51037006). We would like to acknowledge Dr. Haiying Shen (National Center for Nanoscience and Technology of China) for contribution to the fabrication of microfluidic chip. We acknowledge Xin Wang for her contribution to the computer program of magnetic field control system. We also wish to thank Dr. Qiufeng Ma and Dr. Weidong Pan for their discussions and suggestions in the process of the experiment.

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Correspondence to Tao Song.

Electronic supplementary material

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(Online Resource 3) The movie describes that MO-1 microrobots which were not loaded with S. aureus swam from pool M to pool S in a microfluidic chip under the control of applied magnetic field. It corresponds to the process of Fig. 5(a). (MPG 9690 kb)

(Online Resource 4) The video showed that MO-1 microrobots has transported S. aureus from pool S to pool D under the control. It corresponds to the process of Fig. 5(b-e). (MPG 6330 kb)

ESM 1 (Online Resource 1 and Online Resource 2)

(DOCX 650 kb)


(Online Resource 3) The movie describes that MO-1 microrobots which were not loaded with S. aureus swam from pool M to pool S in a microfluidic chip under the control of applied magnetic field. It corresponds to the process of Fig. 5(a). (MPG 9690 kb)


(Online Resource 4) The video showed that MO-1 microrobots has transported S. aureus from pool S to pool D under the control. It corresponds to the process of Fig. 5(b-e). (MPG 6330 kb)

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Chen, C., Chen, C., Yi, Y. et al. Construction of a microrobot system using magnetotactic bacteria for the separation of Staphylococcus aureus . Biomed Microdevices 16, 761–770 (2014).

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  • Magnetotactic bacteria
  • Staphylococcus aureus
  • Microfluidic chip
  • Microrobot
  • Separation