Please wait a minute...

中国生物工程杂志

China Biotechnology
China Biotechnology  2018, Vol. 38 Issue (9): 74-80    DOI: 10.13523/j.cb.20180911
Orginal Article     
Research Progress on Biomedical Applications of Magnetotactic Bacteria and the Biosynthetic Magnetosomes
Fang-xu WANG1,2,Yu-ling CHEN1,2,Du-yan GENG1,Chuan-fang CHEN2,**()
1 State Key Laboratory of Reliability and Intelligence of Electrical Equipment, Hebei University of Technology,Tianjin 300130, China
2 Beijing Key Laboratory of Bioelectromagnetism, Institute of Electrical Engineering, Chinese Academy of Sciences, Beijing 100190, China
Download: HTML   PDF(548KB) HTML
Export: BibTeX | EndNote (RIS)      

Abstract  

In recent years, magnetotactic bacteria and their biosynthetic magnetosomes have been recognized and have been used in biological and medical applications by people because of their good biosafety. Compared with synthetic magnetic nanoparticles, magnetosomes extracted from magnetotactic bacteria have biomembrane coated, high biocompatibility, uniform particle size and high magnetic. Because magnetotactic bacteria swam along magnetic field, they are also applied in biomedical applications. The characterization of magnetotactic bacterium and magnetosome are first descripted, then reviewed their apllications in biomedical in latest research progress.



Key wordsMagnetotactic bacteria      Magnetosomes      Magnetic nanoparticles      Biomedical applications     
Received: 08 May 2018      Published: 12 October 2018
Corresponding Authors: Chuan-fang CHEN     E-mail: chenchf@mail.iee.ac.cn
Cite this article:

Fang-xu WANG,Yu-ling CHEN,Du-yan GENG,Chuan-fang CHEN. Research Progress on Biomedical Applications of Magnetotactic Bacteria and the Biosynthetic Magnetosomes. China Biotechnology, 2018, 38(9): 74-80.

URL:

https://manu60.magtech.com.cn/biotech/10.13523/j.cb.20180911     OR     https://manu60.magtech.com.cn/biotech/Y2018/V38/I9/74

[1]   Sawdon A, Weydemeyer E, Peng C A . Antitumor therapy using nanomaterial-mediated thermolysis. Journal of Biomedical Nanotechnology, 2014,10(9):1894-1917.
doi: 10.1166/jbn.2014.1917
[2]   Wang P, Mao H . The application of nanomaterials in biomedical detection. China Biotechnology, 2011,31(9):88-95.
[3]   Sharma H S, Menon P K, Lafuente J V , et al. The role of functionalized magnetic iron oxide nanoparticles in the central nervous system injury and repair: new potentials for neuroprotection with cerebrolysin therapy. J Nanosci Nanotechnol, 2014,14(1):577-595.
doi: 10.1166/jnn.2014.9213
[4]   Mou X, Ali Z, Li S , et al. Applications of magnetic nanoparticles in targeted drug delivery system. J Nanosci Nanotechnol, 2015,15(1):54-62.
doi: 10.1166/jnn.2015.9585
[5]   Lin M, Huang J, Sha M . Recent advances in nanosized Mn-Zn ferrite magnetic fluid hyperthermia for cancer treatment. J Nanosci Nanotechnol, 2014,14(1):792-802.
doi: 10.1166/jnn.2014.9135
[6]   Alphandery E . Applications of magnetosomes synthesized by magnetotactic bacteria in medicine. Front Bioeng Biotechnol, 2014,2:1-5.
[7]   Yan L, Zhang S, Chen P , et al. Magnetotactic bacteria, magnetosomes and their application. Microbiol Res, 2012,167(9):507-519.
doi: 10.1016/j.micres.2012.04.002
[8]   Blakemore R . Magnetotactic bacteria. Science, 1975,190(4212):377-379.
doi: 10.1126/science.170679
[9]   Jozefczak A, Leszczynski B, Skumiel A , et al. A comparison between acoustic properties and heat effects in biogenic (magnetosomes) and abiotic magnetite nanoparticle suspensions. J Magn Magn Mater, 2016,407:92-100.
doi: 10.1016/j.jmmm.2016.01.054
[10]   Alphandéry E . Applications of magnetosomes synthesized by magnetotactic bacteria in medicine. Frontiers in Bioengineering & Biotechnology, 2014,2(2):5.
[11]   Blakemore R P, Maratea D, Wolfe R S . Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol, 1979,140(2):720-729.
[12]   Simmons S L, Sievert S M, Frankel R B , et al. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl Environ Microbiol, 2004,70(10):6230-6239.
doi: 10.1128/AEM.70.10.6230-6239.2004
[13]   Blakemore R P, Maratea D, Wolfe R S . Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. J Bacteriol, 1979,140(2):720-729.
[14]   Schleifer K H, Schuler D, Spring S , et al. The genus Magnetospirillum Gen-Nov - description of Magnetospirillum-Gryphiswaldense Sp-Nov and transfer of Aquaspirillum-Magnetotacticum to Magnetospirillum-Magnetotacticum Comb-Nov. Syst Appl Microbiol, 1991,14(4):379-385.
doi: 10.1016/S0723-2020(11)80313-9
[15]   Matsunaga T, Sakaguchi T, Tadokoro F . Magnetite formation by a magnetic bacterium capable of growing aerobically. Appl Microbiol Biot, 1991,35(5):651-655.
[16]   Bazylinski D A, Frankel R B, Jannasch H W . Anaerobic magnetite production by a marine, magnetotactic bacterium. Nature, 1988,334(6182):518-519.
doi: 10.1038/334518a0
[17]   Frankel R B, Bazyinski D A, Johnson M S , et al. Magneto-aerotaxis in marine coccoid bacteria. Biophys J, 1997,73(2):994-1000.
doi: 10.1016/S0006-3495(97)78132-3
[18]   Zhu K, Pan H, Li J , et al. Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Res Microbiol, 2010,161(4):276-283.
doi: 10.1016/j.resmic.2010.02.003
[19]   Bazylinski D A, Frankel R B, Heywood B R , et al. Controlled biomineralization of magnetite (Fe3O4) and greigite (Fe3S4) in a magnetotactic bacterium. Appl Environ Microb, 1995,61(9):3232-3239.
[20]   Jacob J J, Suthindhindhiran K . Magnetotactic bacteria and magnetosomes - scope and challenges. Mat Sci Eng C -Mater, 2016,68:919-928.
[21]   Bazylinski D A, Frankel R B . Magnetosome formation in prokaryotes. Nat Rev Microbiol, 2004,2(3):217-230.
doi: 10.1038/nrmicro842
[22]   Arató, Szányi B , Flies Z , et al. Crystal-size and shape distributions of magnetite from uncultured magnetotactic bacteria as a potential biomarker. American Mineralogist, 2005,90(8-9):1233-1240.
doi: 10.2138/am.2005.1778
[23]   Pan Y, Deng C, Liu Q , et al. Biomineralization and magnetism of bacterial magnetosomes. Chinese Science Bulletin, 2004,49(24):2563-2568.
doi: 10.1360/982004-153
[24]   Jogler C, Schüler D . Genomics, genetics, and cell biology of magnetosome formation - annual review of microbiology. Annual Review of Microbiology, 2009,63(1):501.
doi: 10.1146/annurev.micro.62.081307.162908
[25]   Lower B H, Bazylinski D A . The bacterial magnetosome: a unique prokaryotic organelle. J Mol Microbiol Biotechnol, 2013,23(1-2):63-80.
doi: 10.1159/000346543
[26]   Tanaka M, Okamura Y, Arakaki A , et al. Origin of magnetosome membrane: proteomic analysis of magnetosome membrane and comparison with cytoplasmic membrane. Proteomics, 2010,6(19):5234-5247.
[27]   Grünberg K, Müller E C, Otto A , et al. Biochemical and proteomic analysis of the magnetosome membrane in Magnetospirillum gryphiswaldense. Applied & Environmental Microbiology, 2004,70(2):1040.
[28]   Matsunaga T, Okamura Y, Fukuda Y , et al. Complete genome Sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Research, 2005,12(3):157-166.
doi: 10.1093/dnares/dsi002
[29]   Guo F, Liu Y, Chen Y , et al. A novel rapid and continuous procedure for large-scale purification of magnetosomes from Magnetospirillum gryphiswaldense. Applied Microbiology & Biotechnology, 2011,90(4):1277-1283.
[30]   Liu Y, Li G R, Guo F F , et al. Large-scale production of magnetosomes by chemostat culture of Magnetospirillum gryphiswaldense at high cell density. Microbial Cell Factories, 2010,9(1):99.
doi: 10.1186/1475-2859-9-99
[31]   Martel S, Tremblay C C, Ngakeng S , et al. Controlled manipulation and actuation of micro-objects with magnetotactic bacteria. Applied Physics Letters, 2006,89(23):233904-233913.
doi: 10.1063/1.2402221
[32]   Martel S, Mohammadi M . Using a swarm of self-propelled natural microrobots in the form of flagellated bacteria to perform complex micro-assembly tasks//IEEE, IEEE International Conference on Robotics and Automation. 2013: 500-505.
[33]   Felfoul O, Mohammadi M, Taherkhani S , et al. Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions. Nat Nanotechnol, 2016,11(11):941-947.
doi: 10.1038/nnano.2016.137
[34]   Chen C Y, Chen C F, Yi Y , et al. Construction of a microrobot system using magnetotactic bacteria for the separation of Staphylococcus aureus. Biomed Microdevices, 2014,16(5):761-770.
doi: 10.1007/s10544-014-9880-2
[35]   Chen C Y, Chen L J, Wang P P , et al. Magnetically-induced elimination of Staphylococcus aureus by magnetotactic bacteria under a swing magnetic field. Nanomed-Nanotechnol, 2017,13(2):363-370.
doi: 10.1016/j.nano.2016.08.021
[36]   Chen C, Chen L, Yi Y , et al. Evaluation of the anti- Staphylococcus aureus activity of magnetotactic bacteria-mediated magnetic hyperthermia. Applied & Environmental Microbiology, 2016, 82(7): AEM. 04103-15.
[37]   Gobbo O L, Sjaastad K, Radomski M W , et al. Magnetic nanoparticles in cancer theranostics. Theranostics, 2015,5(11):1249-1263.
doi: 10.7150/thno.11544
[38]   Sung B, Shaffer S, Sittek M , et al. Alternating magnetic field-responsive hybrid gelatin microgels for controlled drug release. Jove J Vis Exp, 2016, ( 108):e53680.
[39]   Timko M, Dzarova A, Kovac J , et al. Magnetic properties and heating effect in bacterial magnetic nanoparticles. Journal of Magnetism & Magnetic Materials, 2009,321(10):1521-1524.
[40]   Martinez-Boubeta C, Simeonidis K, Makridis A , et al. Learning from nature to improve the heat generation of iron-oxide nanoparticles for magnetic hyperthermia applications. Sci Rep, 2013,3.DOI: 10.1038/srep01652.
doi: 10.1038/srep01652
[41]   Chen C, Ma Q, Jiang W , et al. Phototaxis in the magnetotactic bacterium Magnetospirillum magneticum strain AMB-1 is independent of magnetic fields. Applied Microbiology & Biotechnology, 2011,90(1):269-275.
[42]   Timko M, Molcan M, Hashim A , et al. Hyperthermic effect in suspension of magnetosomes prepared by various methods. IEEE Transactions on Magnetics, 2013,49(1):250-254.
doi: 10.1109/TMAG.2012.2224098
[43]   Le Fever R, Durand-Dubief M, Chebbi I , et al. Enhanced antitumor efficacy of biocompatible magnetosomes for the magnetic hyperthermia treatment of glioblastoma. Theranostics, 2017,7(18):4618-4631.
doi: 10.7150/thno.18927
[44]   Alphandéry E, Carvallo C, Menguy N , et al. Chains of cobalt doped magnetosomes extracted from AMB-1 magnetotactic bacteria for application in alternative magnetic field cancer therapy. J Phys Chem C, 2011,115(24):11920-11924.
doi: 10.1021/jp201274g
[45]   Alphandéry E, Faure S, Seksek O , et al. Chains of magnetosomes extracted from AMB-1 magnetotactic bacteria for application in alternative magnetic field cancer therapy. Acs Nano, 2011,5(8):6279-6296.
doi: 10.1021/nn201290k
[46]   Alphandéry E, Faure S, Raison L , et al. Heat production by bacterial magnetosomes exposed to an oscillating magnetic field. J Phys Chem C, 2011,115(1):18-22.
doi: 10.1021/jp104580t
[47]   Dikomey E, Franzke J . Effect of heat on induction and repair of DNA strand breaks in X-irradiated Cho cells. Int J Radiat Biol, 1992,61(2):221-233.
doi: 10.1080/09553009214550851
[48]   Maier-Hauff K, Rothe R, R, Gnevechow U , et al. Intracranial thermotherapy using magnetic nanoparticles combined with external beam radiotherapy: results of a feasibility study on patients with glioblastoma multiforme. J Neurooncol, 2007,81(1):53-60.
doi: 10.1007/s11060-006-9195-0
[49]   Alphandéry E, Guyot F, Chebbi I . Preparation of chains of magnetosomes, isolated from Magnetospirillum magneticum strain AMB-1 magnetotactic bacteria, yielding efficient treatment of tumors using magnetic hyperthermia. Int J Pharm, 2012,434(1-2):444-452.
doi: 10.1016/j.ijpharm.2012.06.015
[50]   Alphandéry E, Idbaih A, Adam C , et al. Chains of magnetosomes with controlled endotoxin release and partial tumor occupation induce full destruction of intracranial U87-Luc glioma in mice under the application of an alternating magnetic field. J Control Release, 2017,262:259-272.
doi: 10.1016/j.jconrel.2017.07.020
[51]   Alphandéry E, Idbaih A, Adam C , et al. Development of non-pyrogenic magnetosome minerals coated with poly-l-lysine leading to full disappearance of intracranial U87-Luc glioblastoma in 100% of treated mice using magnetic hyperthermia. Biomaterials, 2017,141:210-222.
doi: 10.1016/j.biomaterials.2017.06.026
[52]   Yang K, Yang G B, Chen L , et al. FeS nanoplates as a multifunctional nano-theranostic for magnetic resonance imaging guided photothermal therapy. Biomaterials, 2015,38:1-9.
doi: 10.1016/j.biomaterials.2014.10.052
[53]   Chu M Q, Shao Y X, Peng J L , et al. Near-infrared laser light mediated cancer therapy by photothermal effect of Fe3O4 magnetic nanoparticles. Biomaterials, 2013,34(16):4078-4088.
doi: 10.1016/j.biomaterials.2013.01.086
[54]   Shen S, Wang S, Zheng R , et al. Magnetic nanoparticle clusters for photothermal therapy with near-infrared irradiation. Biomaterials, 2015,39:67-74.
doi: 10.1016/j.biomaterials.2014.10.064
[55]   Chen C F, Wang S H, Li L L , et al. Bacterial magnetic nanoparticles for photothermal therapy of cancer under the guidance of MRI. Biomaterials, 2016,104:352-360.
doi: 10.1016/j.biomaterials.2016.07.030
[56]   Plan Sangnier A, Preveral S, Curcio A , et al. Targeted thermal therapy with genetically engineered magnetite magnetosomes@RGD: photothermia is far more efficient than magnetic hyperthermia. J Control Release, 2018,279:271-281.
doi: 10.1016/j.jconrel.2018.04.036
[57]   Reddy L H, Arias J L, Nicolas J , et al. Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chemical Reviews, 2012,112(11):5818-5878.
doi: 10.1021/cr300068p
[58]   Chen C F, Wang P P, Li L L . Applications of bacterial magnetic nanoparticles in nanobiotechnology. J Nanosci Nanotechno, 2016,16(3):2164-2171.
doi: 10.1166/jnn.2016.10954
[59]   Xiang L, Wang B, Jin H , et al. Bacterial magnetic particles (BMPs)‐PEI as a novel and efficient non‐viral gene delivery system. Journal of Gene Medicine, 2010,9(8):679-690.
[60]   Sun J B, Duan J H, Dai S L , et al. Preparation and anti-tumor efficiency evaluation of doxorubicin-loaded bacterial magnetosomes: magnetic nanoparticles as drug carriers isolated from Magnetospirillum gryphiswaldense. Biotechnol Bioeng, 2008,101(6):1313-1320.
doi: 10.1002/bit.v101:6
[61]   Sun J B, Duan J H, Dai S L , et al. 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 Lett, 2007,258(1):109-117.
doi: 10.1016/j.canlet.2007.08.018
[62]   Guo L, Huang J, Zheng L M . Control generating of bacterial magnetic nanoparticle-doxorubicin conjugates by poly-L-glutamic acid surface modification. Nanotechnology, 2011,22(17):175102.
doi: 10.1088/0957-4484/22/17/175102
[63]   Tang Y S, Wang D, Zhou C , et al. Bacterial magnetic particles as a novel and efficient gene vaccine delivery system. Gene Ther, 2012,19(12):1187-1195.
doi: 10.1038/gt.2011.197
[64]   Dai Q L, Long R M, Wang S B , et al. Bacterial magnetosomes as an efficient gene delivery platform for cancer theranostics. Microb Cell Fact, 2017,16(1):216.
doi: 10.1186/s12934-017-0830-6
[65]   Cheng L, Ke Y Q, Yu S S , et al. Co-delivery of doxorubicin and recombinant plasmid pHSP70-Plk1-shRNA by bacterial magnetosomes for osteosarcoma therapy. Int J Nanomed, 2016,11:5277-5286.
doi: 10.2147/IJN
[66]   Meriaux S, Boucher M, Marty B , et al. Magnetosomes, biogenic magnetic nanomaterials for brain molecular imaging with 17.2 T MRI scanner. Adv Healthc Mater, 2015,4(7):1076-1083.
doi: 10.1002/adhm.v4.7
[67]   Faivre D, Schuler D . Magnetotactic bacteria and magnetosomes. Chemical Reviews, 2008,108(11):4875-4898.
doi: 10.1021/cr078258w
[68]   Mahmoudi M, Tachibana A, Goldstone A B , et al. Novel MRI contrast agent from magnetotactic bacteria enables in vivo tracking of iPSC-derived cardiomyocytes. Sci Rep-Uk, 2016,6:26960.
doi: 10.1038/srep26960
[69]   Tang T, Zhang L, Gao R , et al. Fluorescence imaging and targeted distribution of bacterial magnetic particles in nude mice. Appl Microbiol Biotechnol, 2012,94(2):495-503.
doi: 10.1007/s00253-012-3981-8
[70]   Boucher M, Geffroy F, Preveral S , et al. Genetically tailored magnetosomes used as MRI probe for molecular imaging of brain tumor. Biomaterials, 2017,121:167-178.
doi: 10.1016/j.biomaterials.2016.12.013
[71]   Schwarz S, Fernandes F, Sanroman L , et al. Synthetic and biogenic magnetite nanoparticles for tracking of stem cells and dendritic cells. J Magn Magn Mater, 2009,321(10):1533-1538.
doi: 10.1016/j.jmmm.2009.02.081
[72]   Benoit M R, Mayer D, Barak Y , et al. Visualizing implanted tumors in mice with magnetic resonance imaging using magnetotactic bacteria. Clin Cancer Res, 2009,15(16):5170-5177.
doi: 10.1158/1078-0432.CCR-08-3206
[73]   Xiang Z C, Yang X L, Xu J J , et al. Tumor detection using magnetosome nanoparticles functionalized with a newly screened EGFR/HER2 targeting peptide. Biomaterials, 2017,115:53-64.
doi: 10.1016/j.biomaterials.2016.11.022
[74]   Aihua L I, Tang T, Zhang H , et al. Modification of bacterial magnetosomes and application of magnetosome-antibody complex in pathogen detection. Acta Biophysica Sinica, 2010,26(8):680-690.
[75]   Peng Z, Ling M, Ning Y , et al. Rapid fluorescent detection of Escherichia coli K88 based on DNA aptamer library as direct and specific reporter combined with immuno-magnetic separation. Journal of Fluorescence, 2014,24(4):1159-1168.
doi: 10.1007/s10895-014-1396-x
[76]   Huang J, Guo L, Zheng L M . Rapid enrichment and determination of phosphopeptides using bacterial magnetic particles via both strong and weak interactions. Analyst, 2010,135(3):559-563.
doi: 10.1039/b920985a
[77]   Wacker R, Ceyhan B, Alhorn P , et al. Magneto immuno-PCR: a novel immunoassay based on biogenic magnetosome nanoparticles. Biochem Bioph Res Co, 2007,357(2):391-396.
doi: 10.1016/j.bbrc.2007.03.156
[78]   Li A H, Zhang H Y, Zhang X , et al. Rapid separation and immunoassay for low levels of Salmonella in foods using magnetosome-antibody complex and real-time fluorescence quantitative PCR. J Sep Sci, 2010,33(21):3437-3443.
doi: 10.1002/jssc.v33:21
[79]   Xu J, Hu J Y, Liu L Z , et al. Surface expression of protein A on magnetosomes and capture of pathogenic bacteria by magnetosome/antibody complexes. Front Microbiol, 2014,5(2):136.
[1] FANG Yuan,ZHANG Tong-wei,CAO Chang-qian,TIAN Jie-sheng,LIN Wei. Diversity and Applications of Magnetotactic Bacteria[J]. China Biotechnology, 2019, 39(12): 73-82.
[2] CHEN Xiao-li, ZOU Ming-yuan, XIE Xin, WANG Sheng-yu, WU Ting, SU Jin-hua. Construction of a Neotype Controllability Magnetic Targeting Restructuring Truncated Tissue Factor[J]. China Biotechnology, 2017, 37(9): 60-64.
[3] WANG Ping, MAO Hong-ju. The Application of Nanomaterials in Biomedical Detection[J]. China Biotechnology, 2011, 31(9): 88-95.