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Optical magnetic imaging of living cells

Abstract

Magnetic imaging is a powerful tool for probing biological and physical systems. However, existing techniques either have poor spatial resolution compared to optical microscopy and are hence not generally applicable to imaging of sub-cellular structure (for example, magnetic resonance imaging1), or entail operating conditions that preclude application to living biological samples while providing submicrometre resolution (for example, scanning superconducting quantum interference device microscopy2, electron holography3 and magnetic resonance force microscopy4). Here we demonstrate magnetic imaging of living cells (magnetotactic bacteria) under ambient laboratory conditions and with sub-cellular spatial resolution (400 nanometres), using an optically detected magnetic field imaging array consisting of a nanometre-scale layer of nitrogen–vacancy colour centres implanted at the surface of a diamond chip. With the bacteria placed on the diamond surface, we optically probe the nitrogen–vacancy quantum spin states and rapidly reconstruct images of the vector components of the magnetic field created by chains of magnetic nanoparticles (magnetosomes) produced in the bacteria. We also spatially correlate these magnetic field maps with optical images acquired in the same apparatus. Wide-field microscopy allows parallel optical and magnetic imaging of multiple cells in a population with submicrometre resolution and a field of view in excess of 100 micrometres. Scanning electron microscope images of the bacteria confirm that the correlated optical and magnetic images can be used to locate and characterize the magnetosomes in each bacterium. Our results provide a new capability for imaging bio-magnetic structures in living cells under ambient conditions with high spatial resolution, and will enable the mapping of a wide range of magnetic signals within cells and cellular networks5,6.

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Figure 1: Wide-field magnetic imaging microscope.
Figure 2: Wide-field optical and magnetic images of magnetotactic bacteria.
Figure 3: Determining magnetic moments of individual bacteria from measured magnetic field distributions.
Figure 4: Localization of magnetic nanoparticle chains using magnetic field measurements.

References

  1. 1

    Lee, S.-C. et al. MR microscopy of micron scale structures. Magn. Reson. Imaging 27, 828–833 (2009)

    CAS  Article  Google Scholar 

  2. 2

    Finkler, A. et al. Self-aligned nanoscale SQUID on a tip. Nano Lett. 10, 1046–1049 (2010)

    CAS  ADS  Article  Google Scholar 

  3. 3

    Dunin-Borkowski, R. E. et al. Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282, 1868–1870 (1998)

    CAS  ADS  Article  Google Scholar 

  4. 4

    Degen, C. L., Poggio, M., Mamin, H. J., Rettner, C. T. & Rugar, D. Nanoscale magnetic resonance imaging. Proc. Natl Acad. Sci. USA 106, 1313–1317 (2009)

    CAS  ADS  Article  Google Scholar 

  5. 5

    Hall, L. T. et al. Monitoring ion-channel function in real time through quantum decoherence. Proc. Natl Acad. Sci. USA 107, 18777–18782 (2010)

    CAS  ADS  Article  Google Scholar 

  6. 6

    Pham, L. M. et al. Magnetic field imaging with nitrogen-vacancy ensembles. N. J. Phys. 13, 045021 (2011)

    Article  Google Scholar 

  7. 7

    Maze, J. R. et al. Nanoscale magnetic sensing with an individual electronic spin in diamond. Nature 455, 644–647 (2008)

    CAS  ADS  Article  Google Scholar 

  8. 8

    Balasubramanian, G. et al. Nanoscale imaging magnetometry with diamond spins under ambient conditions. Nature 455, 648–651 (2008)

    CAS  ADS  Article  Google Scholar 

  9. 9

    Maletinsky, P. et al. A robust scanning diamond sensor for nanoscale imaging with single nitrogen-vacancy centres. Nature Nanotechnol. 7, 320–324 (2012)

    CAS  ADS  Article  Google Scholar 

  10. 10

    Steinert, S. et al. High sensitivity magnetic imaging using an array of spins in diamond. Rev. Sci. Instrum. 81, 043705 (2010)

    CAS  ADS  Article  Google Scholar 

  11. 11

    Le. Sage, D. et al. Efficient photon detection from color centers in a diamond optical waveguide. Phys. Rev. B 85, 121202(R) (2012)

  12. 12

    Hanson, R., Mendoza, F. M., Epstein, R. J. & Awschalom, D. D. Polarization and readout of coupled single spins in diamond. Phys. Rev. Lett. 97, 087601 (2006)

    CAS  ADS  Article  Google Scholar 

  13. 13

    Childress, L. et al. Coherent dynamics of coupled electron and nuclear spin qubits in diamond. Science 314, 281–285 (2006)

    CAS  ADS  Article  Google Scholar 

  14. 14

    Mamin, H. J. et al. Nanoscale nuclear magnetic resonance with a nitrogen-vacancy spin sensor. Science 339, 557–560 (2013)

    CAS  ADS  Article  Google Scholar 

  15. 15

    Staudacher, T. et al. Nuclear magnetic resonance spectroscopy on a (5-nanometer)3 sample volume. Science 339, 561–563 (2013)

    CAS  ADS  Article  Google Scholar 

  16. 16

    Grinolds, M. S. et al. Nanoscale magnetic imaging of a single electron spin under ambient conditions. Nature Phys. 9, 215–219 (2013)

    Google Scholar 

  17. 17

    Komeili, A. Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria. FEMS Microbiol. Rev. 36, 232–255 (2012)

    CAS  Article  Google Scholar 

  18. 18

    Faivre, D. & Schüler, D. Magnetotactic bacteria and magnetosomes. Chem. Rev. 108, 4875–4898 (2008)

    CAS  Article  Google Scholar 

  19. 19

    Lam, K. P. et al. Characterizing magnetism of individual magnetosomes by X-ray magnetic circular dichroism in a scanning transmission X-ray microscope. Chem. Geol. 270, 110–116 (2010)

    CAS  ADS  Article  Google Scholar 

  20. 20

    Qian, L. et al. Magnetic characterization of individual magnetotactic bacteria. (APS March Meeting 2011, 2011); http://meetings.aps.org/link/BAPS.2011.MAR.D16.8 (abstract published online, 2011)

  21. 21

    Proksch, R. B. et al. Magnetic force microscopy of the submicron magnetic assembly in a magnetotactic bacterium. Appl. Phys. Lett. 66, 2582–2584 (1995)

    CAS  ADS  Article  Google Scholar 

  22. 22

    Matsunaga, T., Suzuki, T., Tanaka, M. & Arakaki, A. Molecular analysis of magnetotactic bacteria and development of functional bacterial magnetic particles for nano-biotechnology. Trends Biotechnol. 25, 182–188 (2007)

    CAS  Article  Google Scholar 

  23. 23

    Draper, O. et al. MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ. Mol. Microbiol. 82, 342–354 (2011)

    CAS  Article  Google Scholar 

  24. 24

    Krichevsky, A. et al. Trapping motile magnetotactic bacteria with a magnetic recording head. J. Appl. Phys. 101, 014701 (2007)

    ADS  Article  Google Scholar 

  25. 25

    Moskowitz, B. M., Frankel, R. B. & Bazylinski, D. A. Rock magnetic criteria for the detection of biogenic magnetite. Earth Planet. Sci. Lett. 120, 283–300 (1993)

    ADS  Article  Google Scholar 

  26. 26

    Pósfai, M. & Dunin-Borkowski, R. E. Magnetic nanocrystals in organisms. Elements 5, 235–240 (2009)

    Article  Google Scholar 

  27. 27

    Zurkiya, O., Chan, A. W. S. & Hu, X. Mag A is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn. Reson. Med. 59, 1225–1231 (2008)

    CAS  Article  Google Scholar 

  28. 28

    Dobson, J. Magnetic iron compounds in neurological disorders. Ann. NY Acad. Sci. 1012, 183–192 (2004)

    CAS  ADS  Article  Google Scholar 

  29. 29

    Mora, C. V., Davison, M., Wild, J. M. & Walker, M. M. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508–511 (2004)

    CAS  ADS  Article  Google Scholar 

  30. 30

    Eder, S. H. K. et al. Magnetic characterization of isolated candidate vertebrate magnetoreceptor cells. Proc. Natl Acad. Sci. USA 109, 12022–12027 (2012)

    CAS  ADS  Article  Google Scholar 

  31. 31

    Komeili, A., Vali, H., Beveridge, T. J. & Newman, D. K. Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation. Proc. Natl Acad. Sci. USA 101, 3839–3844 (2004)

    CAS  ADS  Article  Google Scholar 

  32. 32

    Murat, D., Quinlan, A., Vali, H. & Komeili, A. Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proc. Natl Acad. Sci. USA 107, 5593–5598 (2010)

    CAS  ADS  Article  Google Scholar 

Download references

Acknowledgements

We thank L. Qian for discussions about related experiments using a scanning SQUID microscope in the laboratory of K. A. Moler, J. W. Lichtman and R. Schalek for access to the SEM, S. G. Turney for access to the water-immersion objective and advice regarding cell immobilization, and P. R. Hemmer and H. Park for technical discussions. A.K. was supported by a David and Lucille Packard Foundation Fellowship in Science and Engineering and by the National Institutes of Health (R01GM084122). This work was supported by the NSF and the DARPA QuASAR programme.

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Contributions

D.L. and R.L.W. conceived the idea of the study. K.A. developed modelling and fitting algorithms to interpret the data. D.L., K.A., D.R.G., S.J.D. and L.M.P. performed magnetic, optical and SEM imaging experiments, and analysed data. L.R.-L. and A.K. provided bacteria cultures and TEM images. M.D.L., R.L.W. and A.Y conceived the application of the NV-diamond wide-field imager to biomagnetism. All authors discussed the results and participated in writing the manuscript.

Corresponding author

Correspondence to R. L. Walsworth.

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The authors declare no competing financial interests.

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Le Sage, D., Arai, K., Glenn, D. et al. Optical magnetic imaging of living cells. Nature 496, 486–489 (2013). https://doi.org/10.1038/nature12072

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