Cite this paper:
Tongwei ZHANG, Huangtao XU, Jia LIU, Yongxin PAN, Changqian CAO. Determination of the heating efficiency of magnetotactic bacteria in alternating magnetic field[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2116-2126

Determination of the heating efficiency of magnetotactic bacteria in alternating magnetic field

Tongwei ZHANG1,2,3,4, Huangtao XU1,2,3,4, Jia LIU1,2,4, Yongxin PAN1,2,3,4, Changqian CAO1,2,4
1 Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Innovation Academy for Earth Science, Chinese Academy of Sciences, Beijing 100029, China;
2 Innovation Academy for Earth Science, Chinese Academy of Sciences, Beijing 100029, China;
3 College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing 100049, China;
4 France-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing 100029, China
Abstract:
Magnetotactic bacteria (MTB) intact cells have been applied in magnetic hyperthermia therapy of tumor, showing great efficiency in heating for tumor cell inhibition. However, the detailed magnetic hyperthermia properties and optimum heat production conditions of MTB cells are still poorly understood due to lack of standard measuring equipment. The specific absorption rate (SAR) of MTB cells is often measured by home-made equipment at a limited frequency and magnetic field amplitude. In this study, we have used a commercial standard system to implement a comprehensive study of the hyperthermic response of Magnetospirillum gryphiswaldense MSR-1 strain under 7 frequencies of 144–764 kHz, and 8 field amplitudes between 10 and 45 kA/m. The measurement results prove that the SAR of MTB cells increases with magnetic field frequency and amplitude within a certain range. In combination with the magnetic measurements, it is determined that the magnetic hyperthermia mechanism of MTB mainly follows the principle of hysteresis loss, and the heat efficiency of MTB cells in alternating magnetic field are mainly affected by three parameters of hysteresis loop, saturation magnetisation, saturation remanent magnetisation, and coercivity. Thus when we culture MTB in LA-2 medium containing sodium nitrate as source of nitrogen, the SAR of MTBLA-2 cells with magnetosomes arranged in chains can be as high as 4 925.6 W/g (in this work, all SARs are calculated with iron mass) under 764 kHz and 30 kA/m, which is 7.5 times than current commercial magnetic particles within similar size range.
Key words:    magnetotactic bacteria (MTB)|hyperthermia|rock magnetism|alternating magnetic field (AMF)   
Received: 2021-03-01   Revised: 2021-03-23
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References:
Alphandéry E, Faure S, Raison L, Duguet E, Howse P A, Bazylinski D A. 2011. Heat production by bacterial magnetosomes exposed to an oscillating magnetic field. The Journal of Physical Chemistry C, 115(1):18-22, https://doi.org/10.1021/jp104580t.
Andreu I, Natividad E. 2013. Accuracy of available methods for quantifying the heat power generation of nanoparticles for magnetic hyperthermia. International Journal of Hyperthermia, 29(8):739-751, https://doi.org/10.3109/02656736.2013.826825.
Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nature Reviews Microbiology, 2(3):217-230, https://doi.org/10.1038/nrmicro842.
Blakemore R. 1975. Magnetotactic bacteria. Science, 190(4212):377-379, https://doi.org/10.1126/science.170679.
Blanco-Andujar C, Teran F J, Ortega D. 2018. Chapter 8:Current Outlook and Perspectives on NanoparticleMediated Magnetic Hyperthermia. Iron Oxide Nanoparticles for Biomedical Applications:Synthesis, Functionalization and Application. Elsevier. p.197-245.
Brezovich I A. 1988. Low frequency hyperthermia:capacitive and ferromagnetic thermoseed methods. Medical Physics Monograph, 16:82-111.
Chen C Y, Chen L J, Wang P P, Wu L F, Song T. 2019. Steering of magnetotactic bacterial microrobots by focusing magnetic field for targeted pathogen killing. Journal of Magnetism and Magnetic Materials, 479:74-83, https://doi.org/10.1016/j.jmmm.2019.02.004.
Dadfar S M, Roemhild K, Drude N I, Von Stillfried S, Knüchel R, Kiessling F, Lammers T. 2019. Iron oxide nanoparticles:diagnostic, therapeutic and theranostic applications. Advanced Drug Delivery Reviews, 138:302-325, https://doi.org/10.1016/j.addr.2019.01.005.
Ding Y, Li J H, Liu J N, Yang J, Jiang W, Tian J S, Li T, Pan Y X, Li J L. 2010. Deletion of the ftsZ-like gene results in the production of superparamagnetic magnetite magnetosomes in Magnetospirillum gryphiswaldense. Journal of Bacteriology, 192(4):1097-1105, https://doi.org/10.1128/JB.01292-09.
Falk M H, Issels R D. 2001. Hyperthermia in oncology. International Journal of Hyperthermia, 17(1):1-18, https://doi.org/10.1080/02656730150201552.
Fdez-Gubieda M L, Alonso J, García-Prieto A, García-Arribas A, Barquín L F, Muela A. 2020. Magnetotactic bacteria for cancer therapy. Journal of Applied Physics, 128(7):070902, https://doi.org/10.1063/5.0018036.
Frankel R B, Bazylinski D A, Johnson M S, Taylor B L. 1997. Magneto-aerotaxis in marine coccoid bacteria. Biophysical Journal, 73(2):994-1000, https://doi.org/10.1016/S0006-3495(97)78132-3.
Gandia D, Gandarias L, Rodrigo I, Robles-García J, Das R, Garaio E, García J Á, Phan M H, Srikanth H, Orue I, Alonso J, Muela A, Gubieda M L F. 2019. Unlocking the potential of magnetotactic bacteria as magnetic hyperthermia agents. Small, 15(41):1902626, https://doi.org/10.1002/smll.201902626.
Han X H, Tomaszewski E J, Sorwat J, Pan Y X, Kappler A, Byrne J M. 2020. Effect of microbial biomass and humic acids on abiotic and biotic magnetite formation. Environmental Science & Technology, 54(7):4121-4130, https://doi.org/10.1021/acs.est.9b07095.
Hergt R, Andra W, d'Ambly C G, Hilger I, Kaiser W A, Richter U, Schmidt H G. 1998. Physical limits of hyperthermia using magnetite fine particles. IEEE Transactions on Magnetics, 34(5):3745-3754, https://doi.org/10.1109/20.718537.
Hergt R, Dutz S, Müller R, Zeisberger M. 2006. Magnetic particle hyperthermia:nanoparticle magnetism and materials development for cancer therapy. Journal of Physics:Condensed Matter, 18(38):S2919, https://doi.org/10.1088/0953-8984/18/38/S26.
Hergt R, Dutz S, Röder M. 2008. Effects of size distribution on hysteresis losses of magnetic nanoparticles for hyperthermia. Journal of Physics:Condensed Matter, 20(38):385214, https://doi.org/10.1088/0953-8984/20/38/385214.
Hergt R, Hiergeist R, Zeisberger M, Schüler D, Heyen U, Hilger I, Kaiser W A. 2005. Magnetic properties of bacterial magnetosomes as potential diagnostic and therapeutic tools. Journal of Magnetism and Magnetic Materials, 293(1):80-86, https://doi.org/10.1016/j.jmmm.2005.01.047.
Heyen U, Schüler D. 2003. Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor. Applied Microbiology and Biotechnology, 61(5):536-544, https://doi.org/10.1007/s00253-002-1219-x.
Johannsen M, Gneveckow U, Thiesen B, Taymoorian K, Cho C H, Waldöfner N, Scholz R, Jordan A, Loening S A, Wust P. 2007. Thermotherapy of prostate cancer using magnetic nanoparticles:feasibility, imaging, and threedimensional temperature distribution. European Urology, 52(6):1653-1662, https://doi.org/10.1016/j.eururo.2006.11.023.
Kallumadil M, Tada M, Nakagawa T, Abe M, Southern P, Pankhurst Q A. 2009. Suitability of commercial colloids for magnetic hyperthermia. Journal of Magnetism and Magnetic Materials, 321(10):1509-1513, https://doi.org/10.1016/j.jmmm.2009.02.075.
Li A H, Tang T, Zhang H Y, Wang Q, Tian J S, Li Y. 2010. Modification of Bacterial magnetosomes and application of magnetosome-antibody complex in pathogen detection. Acta Biophysica Sinica, 26(8):680-690. (in Chinese with English abstract)
Li J H, Liu P Y, Wang J, Roberts A P, Pan Y X. 2020. Magnetotaxis as an adaptation to enable bacterial shuttling of microbial sulfur and sulfur cycling across aquatic oxicanoxic interfaces. Journal of Geophysical Research:Biogeosciences, 125(12):e2020JG006012, https://doi.org/10.1029/2020JG006012.
Li J H, Menguy N, Arrio M A, Sainctavit P, Juhin A, Wang Y Z, Chen H T, Bunau O, Otero E, Ohresser P, Pan Y X. 2016. Controlled cobalt doping in the spinel structure of magnetosome magnetite:new evidences from elementand site-specific X-ray magnetic circular dichroism analyses. Journal of the Royal Society Interface, 13(121):20160355, https://doi.org/10.1098/rsif.2016.0355.
Li J H, Wu W F, Liu Q S, Pan Y X. 2012. Magnetic anisotropy, magnetostatic interactions and identification of magnetofossils. Geochemistry, Geophysics, Geosystems, 13(12):Q10Z51, https://doi.org/10.1029/2012GC004384.
Lin W, Li J H, Schüler D, Jogler C, Pan Y X. 2009. Diversity analysis of magnetotactic bacteria in Lake Miyun, northern China, by restriction fragment length polymorphism. Systematic and Applied Microbiology, 32(5):342-350, https://doi.org/10.1016/j.syapm.2008.10.005.
Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, Orawa H, Budach V, Jordan A. 2011. Efficacy and safety of intratumoral thermotherapy using magnetic ironoxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. Journal of Neuro-Oncology, 103(2):317-324, https://doi.org/10.1007/s11060-010-0389-0.
Mason P A, Hurt W D, Walters T J, D'Andrea J A, Ryan K L, Nelson D A, Smith K I, Ziriax J M. 2000. Effects of frequency, permittivity, and voxel size on predicted specific absorption rate values in biological tissue during electromagnetic-field exposure. IEEE Transactions on Microwave Theory and Techniques, 48(11):2050-2058, https://doi.org/10.1109/22.884194.
Muela A, Muñ oz D, Martin-Rodriguez R, Orue I, Garaio E, de Cerio A A D, Alonso J, García J Á, Fdez-Gubieda M L. 2016. Optimal parameters for hyperthermia treatment using biomineralized magnetite nanoparticles:theoretical and experimental approach. The Journal of Physical Chemistry C, 120(42):24437-24448, https://doi.org/10.1021/acs.jpcc.6b07321.
Ortega D, Pankhurst Q A. 2013. Magnetic hyperthermia. In:P. O'Brien. Nanoscience:Volume 1:Nanostructures through Chemistry. Royal Society of Chemistry:Cambridge. p.60-88, https://doi.org/10.1039/9781849734844-00060.
Pankhurst Q A, Connolly J, Jones S K, Dobson J. 2003. Applications of magnetic nanoparticles in biomedicine. Journal of Physics D:Applied Physics, 36(13):R167, https://doi.org/10.1088/0022-3727/36/13/201.
Périgo E A, Hemery G, Sandre O, Ortega D, Garaio E, Plazaola F, Teran F J. 2015. Fundamentals and advances in magnetic hyperthermia. Applied Physics Reviews, 2(4):041302, https://doi.org/10.1063/1.4935688.
Rosensweig R E. 2002. Heating magnetic fluid with alternating magnetic field. Journal of Magnetism and Magnetic Materials, 252:370-374, https://doi.org/10.1016/S0304-8853(02)00706-0.
Schüler D, Uhl R, Bäuerlein E. 1995. A simple light scattering method to assay magnetism in Magnetospirillum gryphiswaldense. FEMS Microbiology Letters, 132(1-2):139-145, https://doi.org/10.1111/j.1574-6968.1995.tb07823.x.
Stookey L L. 1970. Ferrozine-a new spectrophotometric reagent for iron. Analytical Chemistry, 42(7):779-781, https://doi.org/10.1021/ac60289a016.
Sun J B, Duan J H, Dai S L, Ren J, Zhang Y D, Tian J S, Li Y. 2007. In vitro and in vivo antitumor effects of doxorubicin loaded with bacterial magnetosomes (DBMs) on H22 cells:the magnetic bio-nanoparticles as drug carriers. Cancer Letters, 258(1):109-117, https://doi.org/10.1016/j.canlet.2007.08.018.
Sun J B, Zhao F, Tang T, Jiang W, Tian J S, Li Y, Li J L. 2008. High-yield growth and magnetosome formation by Magnetospirillum gryphiswaldense MSR-1 in an oxygencontrolled fermentor supplied solely with air. Applied Microbiology and Biotechnology, 79(3):389-397, https://doi.org/10.1007/s00253-008-1453-y.
Thiesen B, Jordan A. 2008. Clinical applications of magnetic nanoparticles for hyperthermia. International Journal of Hyperthermia, 24(6):467-474, https://doi.org/10.1080/02656730802104757.
Uebe R, Schüler D. 2016. Magnetosome biogenesis in magnetotactic bacteria. Nature Reviews Microbiology, 14(10):621-637, https://doi.org/10.1038/nrmicro.2016.99.
Xu H T, Pan Y X. 2019. Experimental evaluation on the heating efficiency of magnetoferritin nanoparticles in an alternating magnetic field. Nanomaterials, 9(10):1457, https://doi.org/10.3390/nano9101457.
Yang W J, Bai Y, Wang X, Dong X X, Li Y, Fang M Y. 2016. Attaching biosynthesized bacterial magnetic particles to polyethylenimine enhances gene delivery into mammalian cells. Journal of Biomedical Nanotechnology, 12(4):789-799, https://doi.org/10.1166/jbn.2016.2213.
Zhang T W, Pan Y X. 2018. Constraining the magnetic properties of ultrafine-and fine-grained biogenic magnetite. Earth, Planets and Space, 70(1):206, https://doi.org/10.1186/s40623-018-0978-2.
Zhang Y, Zhang X J, Jiang W, Li Y, Li J L. 2011. Semicontinuous culture of Magnetospirillum gryphiswaldense MSR-1 cells in an autofermentor by nutrient-balanced and isosmotic feeding strategies. Applied and Environmental Microbiology, 77(17):5851-5856, https://doi.org/10.1128/AEM.05962-11.
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