Research Progress on the Function and Application of Membrane Protein Mms6 of Magnetosome

doi:10.13560/j.cnki.biotech.bull.1985.2017-0170

Abstract

Abstract: The magnetosome is a special biomineralized product formed by the invagination of the magnetotactic bacteria（MTB）inner membrane. Magnetosome is composed of membrane-enclosed magnetite crystals ordered into chains along the cell. Moreover,these magnetic nanocrystals are highly homogeneous in size and morphology. The magnetosome membrane protein has been demonstrated to play an important role in the formation of magnetosome with recruitment and redox of iron and regulation of the nucleation and growth of magnetic nanocrystals. This article reviews that the main function of protein in magnetosome membrane in the process of the formation of magnetic nanoparticles from the absorption of iron ions into mineralization. Especially,the article introduces the structure characteristics and functions of the magnetosome membrane special protein 6（Mms6）. Furthermore,the article summarizes the application of Mms6,as a biomimic addictive in the new-type magnetic nanomaterials,and discusses its possible mechanism of molecular regulation during the process of the formation of magnetosome,for providing a better understanding of biomineralization.

Key words: magnetosome, biomineralization, mms6 protein, biomimeticsynthesis

MA Kun,ZHAO Hong-xin,LI Qian,WANG Jia-rong,SUN Hong-bin. Research Progress on the Function and Application of Membrane Protein Mms6 of Magnetosome[J]. Biotechnology Bulletin, 2017, 33(9): 48-55.

References

[1] Lu AH, Salabas EEL, Schüth F. Magnetic nanoparticles：synthesis, protection, functionalization, and applicationn[J] . Angewandte Chemie International Editio, 2007, 46（8）：1222-1244.
[2] Goldhawk DE, Rohani R, Sengupta A, et al. Using the magnetosome to model effective gene-based contrast for magnetic resonance imaging[J] . Wiley Interdisciplinary Reviews：Nanomedicine and Nanobiotechnology, 2012, 4（4）：378-388.
[3] Tang Y, Wang D, Zhou C, et al. Bacterial magnetic particles as a novel and efficient gene vaccine delivery system[J] . Gene Therapy, 2012, 19（12）：1187-1195.
[4] Jimenez-Lopez C, Romanek CS, Bazylinski DA. Magnetite as a prokaryotic biomarker：a review[J] . Journal of Geophysical Research：Biogeosciences, 2010, doi：10.102912009fg00152.
[5] Matsunaga T, Okamura Y, Tanaka T. Biotechnological application of nano-scale engineered bacterial magnetic particles[J] . Journal of Materials Chemistry, 2004, 14（14）：2099-2105.
[6] 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[J] . ACS Nano, 2011, 5（8）：6279-6296.
[7] Arakaki A, Nakazawa H, Nemoto M, et al. Formation of magnetite by bacteria and its application[J] . Journal of the Royal Society interface, 2008, 5（26）：977-999.
[8] Xu AW, Ma Y, C?lfen H. Biomimetic mineralization[J] . Journal of Materials Chemistry, 2007, 17（5）：415-449.
[9] Chiu CY, Ruan L, Huang Y. Biomolecular specificity controlled na-nomaterial synthesis[J] . Chemical Society Reviews, 2013, 42（7）：2512-2527.
[10] Lenders JJ, Altan CL, Bomans PH, et al. A bioinspired coprecipitation method for the controlled synthesis of magnetite nanoparticles[J] . Crystal Growth & Design, 2014, 14（11）：5561-5568.
[11] Diebel CE, Proksch R, Green CR, et al. Magnetite defines a vertebrate magnetoreceptor[J] . Nature, 2000, 406（6793）：299-302.
[12] Ueda K, Kusunoki M, Kato M, et al. Magnetic remanences in migratory birds[J] . Journal of the Yamashina Institute for Ornithology, 1982, 14（2-3）：166-170.
[13] Yan L, Zhang S, Chen P, et al. Magnetotactic bacteria, magnetosomes and their application[J] . Microbiological Research, 2012, 167（9）：507-519.
[14] Komeili A. Molecular mechanisms of compartmentalization and biomineralization in magnetotactic bacteria[J] . FEMS Microbiology Reviews, 2012, 36（1）：232-255.
[15] Schüler D. Genetics and cell biology of magnetosome formation in magnetotactic bacteria[J] . FEMS Microbiology Reviews, 2008, 32（4）：654-672.
[16] Nakamura C, Burgess JG, Sode K, et al. An iron-regulated gene, magA, encoding an iron transport protein of Magnetospirillum sp. strain AMB-1[J] . Journal of Biological Chemistry, 1995, 270（47）：28392-28396.
[17] Uebe R, Junge K, Henn V, et al. The cation diffusion facilitator proteins MamB and MamM of Magnetospirillum gryphiswaldense have distinct and complex functions, and are involved in magnetite biomineralization and magnetosome membrane assembly[J] . Molecular Microbiology, 2011, 82（4）：818-835.
[18] Siponen MI, Adryanczyk G, Ginet N, et al. Magnetochrome：a c-type cytochrome domain specific to magnetotatic bacteria[J] . Biochemical Society transactions, 2012, 40（6）：1319-1323.
[19] Tanaka M, Mazuyama E, Arakaki A, et al. MMS6 protein regulates crystal morphology during nano-sized magnetite biomineralization in vivo[J] . Journal of Biological Chemistry, 2011, 286（8）：6386-6392.
[20] Tanaka M, Arakaki A, Matsunaga T. Identification and functional characterization of liposome tubulation protein from magnetotactic bacteria[J] . Molecular microbiology, 2010, 76（2）：480-488.
[21] Zeytuni N, Ozyamak E, Ben-Harush K, et al. Self-recognition mechanism of MamA, a magnetosome-associated TPR-containing protein, promotes complex assembly[J] . Proceedings of the National Academy of Sciences, 2011, 108（33）：E480-E487.
[22] Zeytuni N, Baran D, Davidov G, et al. Inter-phylum structural conservation of the magnetosome-associated TPR-containing protein, MamA[J] . Journal of Structural Biology, 2012, 180（3）：479-487.
[23] Zurkiya O, Chan AW, Hu X. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter[J] . Magnetic Resonance in Medicine, 2008, 59（6）：1225-1231.
[24] Siponen MI, Legrand P, Widdrat M, et al. Structural insight into magnetochrome-mediated magnetite biomineralization[J] . Nature, 2013, 502（7473）：681-684.
[25] Komeili A, Li Z, Newman DK, et al. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK[J] . Science, 2006, 311（5758）：242-245.
[26] Draper O, Byrne ME, Li Z, et al. MamK, a bacterial actin, forms dynamic filaments in vivo that are regulated by the acidic proteins MamJ and LimJ[J] . Molecular Microbiology, 2011, 82（2）：342-354.
[27] Scheffel A, Schüler D. The acidic repetitive domain of the Magneto-spirillum gryphiswaldense MamJ protein displays hypervariability but is not required for magnetosome chain assembly[J] . Journal of Bacteriology, 2007, 189（17）：6437-6446.
[28] Arakaki A, Yamagishi A, Fukuyo A, et al. Co-ordinated functions of Mms proteins define the surface structure of cubo-octahedral magnetite crystals in magnetotactic bacteria[J] . Molecular microbiology, 2014, 93（3）：554-567.
[29] Kolinko I, Lohβe A, Borg S, et al. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters[J] . Nature Nanotechnology, 2014, 9（3）：193-197.
[30] Arakaki A, Webb J, Matsunaga T. A novel protein tightly bound to bacterial magnetic particles in Magnetospirillum magneticum strain AMB-1[J] . Journal of Biological Chemistry, 2003, 278（10）：8745-8750.
[31] Murat D, Falahati V, Bertinetti L, et al. The magnetosome membrane protein, MmsF, is a major regulator of magnetite biomineralization in Magnetospirillum magneticum AMB-1[J] . Molecular Microbiology, 2012, 85（4）：684-699.
[32] Wang L, Prozorov T, Palo PE, et al. Self-assembly and biphasic iron-binding characteristics of Mms6, a bacterial protein that promotes the formation of superparamagnetic magnetite nanoparticles of uniform size and shape[J] . Biomacromolecules, 2011, 13（1）：98-105.
[33] Amemiya Y, Arakaki A, Staniland SS, et al. Controlled formation of magnetite crystal by partial oxidation of ferrous hydroxide in the presence of recombinant magnetotactic bacterial protein Mms6[J] . Biomaterials, 2007, 28（35）：5381-5389.
[34] Zhang H, Liu X, Feng S, et al. Morphological transformations in the magnetite biomineralizing protein Mms6 in iron solutions：a small-angle X-ray scattering study[J] . Langmuir, 2015, 31（9）：2818-2825.
[35] Kashyap S, Woehl TJ, Liu X, et al. Nucleation of iron oxide nanoparticles mediated by Mms6 protein in situ[J] . ACS Nano, 2014, 8（9）：9097-9106.
[36] Ma K, Zhao H, Zheng X, et al. NMR studies of the interactions between AMB-1 Mms6 protein and magnetosome Fe3O4 nanoparticles[J] . Journal of Materials Chemistry B, 2017, 5（16）：2888-2895.
[37] Prozorov T, Palo P, Wang L, et al. Cobalt ferrite nanocrystals：out-performing magnetotactic bacteria[J] . ACS Nano, 2007, 1（3）：228-233.
[38] Arakaki A, Masuda F, Amemiya Y, et al. Control of the morphology and size of magnetite particles with peptides mimicking the Mms6 protein from magnetotactic bacteria[J] . Journal of Colloid and Interface Science, 2010, 343（1）：65-70.
[39] Rawlings AE, Bramble JP, Hounslow AM, et al. Ferrous iron binding key to Mms6 magnetite biomineralisation：A mechanistic study to understand magnetite formation using pH titration and NMR spectroscopy[J] . Chemistry-A European Journal, 2016, 22（23）：7885-7894.
[40] Yamagishi A, Narumiya K, Tanaka M, et al. Core amino acid residues in the morphology-regulating protein, Mms6, for intracellular magnetite biomineralization[J] . Scientific Reports, 2016, 6：35670.
[41] Prozorov T, Mallapragada SK, Narasimhan B, et al. Protein‐mediated synthesis of uniform superparamagnetic magnetite nanocrystals[J] . Advanced Functional Materials, 2007, 17（6）：951-957.
[42] Galloway JM, Arakaki A, Masuda F, et al. Magnetic bacterial protein Mms6 controls morphology, crystallinity and magnetism of cobalt-doped magnetite nanoparticles in vitro[J] . Journal of Materials Chemistry, 2011, 21（39）：15244-15254.
[43] Zhang H, Malik V, Mallapragada S, et al. Synthesis and characteri-zation of Gd-doped magnetite nanoparticles[J] . Journal of Magn-etism and Magnetic Materials, 2017, 423：386-394.
[44] Arakaki A, Kikuchi D, Tanaka M, et al. Comparative subcellular localization analysis of magnetosome proteins reveals a unique localization behavior of Mms6 protein onto magnetite crystals[J] . Journal of Bacteriology, 2016, 198（20）：2794-2802.
[45] Oestreicher Z, Mumper E, Gassman C, et al. Spatial localization of Mms6 during biomineralization of Fe3O4 nanocrystals in Magnetospirillum magneticum AMB-1[J] . Journal of Materials Research, 2016, 31（5）：527-535.
[46] Wolff A, Frese K, Wi?brock M, et al. Influence of the synthetic polypeptide c25-mms6 on cobalt ferrite nanoparticle formation[J] . Journal of Nanoparticle Research, 2012, 14（10）：1161.
[47] Lenders JJ, Zope HR, Yamagishi A, et al. Bioinspired magnetite crystallization directed by random copolypeptides[J] . Advanced Functional Materials, 2015, 25（5）：711-719.
[48] Galloway JM, Bramble JP, Rawlings AE, et al. Biotemplated magnetic nanoparticle arrays[J] . Small, 2012, 8（2）：204-208.
[49] Bird SM, Rawlings AE, Galloway JM, et al. Using a biomimetic membrane surface experiment to investigate the activity of the magnetite biomineralisation protein Mms6[J] . RSC Advances, 2016, 6（9）：7356-7363.
[50] Nayak S, Zhang H, Liu X, et al. Protein patterns template arrays of magnetic nanoparticles[J] . RSC Advances, 2016, 6（62）：57048-57056.
[51] Bird SM, Galloway JM, Rawlings AE, et al. Taking a hard line with biotemplating：cobalt-doped magnetite magnetic nanoparticle arrays[J] . Nanoscale, 2015, 7（16）：7340-7351.
[52] Liu X, Zhang H, Nayak S, et al. Effect of surface hydrophobicity on the function of the immobilized biomineralization protein Mms6[J] . Industrial & Engineering Chemistry Research, 2015, 54（42）：10284-10292.