Magnetic bacterial protein Mms6 controls morphology, crystallinity and magnetism of cobalt-doped magnetite nanoparticles in vitro

Galloway, Johanna M.; Arakaki, Atsushi; Masuda, Fukashi; Tanaka, Tsuyoshi; Matsunaga, Tadashi; Staniland, Sarah S.

doi:10.1039/c1jm12003d

Cited by 62 publications

(86 citation statements)

References 52 publications

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“…To explore the activity of these proteins in vitro, we successfully cloned the genes into expression vectors to produce StrepII tag fusions (sequence WSHPQFEK) to the N termini of the target proteins in Escherichia coli. We selected StrepII tags to avoid possible effects from polyhistidine tags, which are able to bind metal ions during magnetite formation, and have been shown to slightly alter size of formed nanoparticles in synthetic precipitation reactions (18), potentially masking or subtly altering the effect of the protein on the formed particles. The proteins were expressed in E. coli cells, and the presence of tagged protein in the total and soluble proteomes was determined by Western blot analysis with an antibody against the StrepII sequence, as shown in Fig.…”

Section: Resultsmentioning

confidence: 99%

Self-assembled MmsF proteinosomes control magnetite nanoparticle formation in vitro

Rawlings

Bramble

Walker

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Magnetotactic bacteria synthesize highly uniform intracellular magnetite nanoparticles through the action of several key biomineralization proteins. These proteins are present in a unique lipidbound organelle (the magnetosome) that functions as a nanosized reactor in which the particle is formed. A master regulator protein of nanoparticle formation, magnetosome membrane specific F (MmsF), was recently discovered. This predicted integral membrane protein is essential for controlling the monodispersity of the nanoparticles in Magnetospirillum magneticum strain AMB-1. Two MmsF homologs sharing over 60% sequence identity, but showing no apparent impact on particle formation, were also identified in the same organism. We have cloned, expressed, and used these three purified proteins as additives in synthetic magnetite precipitation reactions. Remarkably, these predominantly α-helical membrane spanning proteins are unusually highly stable and water-soluble because they self-assemble into spherical aggregates with an average diameter of 36 nm. The MmsF assembly appears to be responsible for a profound level of control over particle size and iron oxide (magnetite) homogeneity in chemical precipitation reactions, consistent with its indicated role in vivo. The assemblies of its two homologous proteins produce imprecise various iron oxide materials, which is a striking difference for proteins that are so similar to MmsF both in sequence and hierarchical structure. These findings show MmsF is a significant, previously undiscovered, protein additive for precision magnetite nanoparticle production. Furthermore, the self-assembly of these proteins into discrete, soluble, and functional "proteinosome" structures could lead to advances in fields ranging from membrane protein production to drug delivery applications.MmsF | proteinosome | magnetite | magnetosome | in vitro precipitation M agnetic nanoparticles (MNPs) represent an area of intense research due to their diverse and pertinent applications across a range of disciplines and industries. Applications for MNPs include biomedical diagnostics and therapies (1-3), such as MRI contrast reagents, tumor hyperthermia treatments, and magnetically targeted drug delivery, as well as data storage (4) and biotechnology. However, specific magnetic and physical properties of MNPs are critical to the success of each application, with specific size and morphology (with a narrow distribution) being essential considerations. Pure magnetite MNP synthesis under ambient conditions is notoriously difficult to control, with simple precipitations often resulting in a mixture of differently sized and shaped particles with other iron oxide contaminants. This situation can be improved somewhat by using more extreme processes, such as high-temperature incubations or capping surfactants, which favor certain MNP types (5, 6). However, the use of toxic or organic reagents and extreme conditions comes with a high energy and monetary cost, and can limit the biocompatibility of the MNPs for subsequent app...

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Section: Resultsmentioning

confidence: 99%

Self-assembled MmsF proteinosomes control magnetite nanoparticle formation in vitro

Rawlings

Bramble

Walker

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…18 Therefore, significant research efforts have led to understanding the mechanism of Mms6 biomineralization in vivo, 16 synthesizing a variety of magnetic nanomaterials in vitro, and thereby expanding the biomineralization processes beyond natural materials. 22,25,26 Progress has been made recently in understanding the structure and properties of Mms6. 21,27 Mms6 is an amphiphilic protein with hydrophobic N-terminal and hydrophilic C-terminal, is believed to exist as a membrane protein in vivo, and selfassembles in vitro to form a multimeric micellar complex larger than 300 kDa.…”

Section: ■ Introductionmentioning

confidence: 99%

“…It is worth noting that the concentrations of proteins subjected to SAXS measurements are increased to the level of ∼1 mg/mL in order to achieve acceptable data quality, while most reported Mms6 concentrations used for magnetic nanocrystal synthesis are less than 0.07 mg/mL to use the minimal amount of protein needed to facilitate nanocrystal formation. 15,20,21,25 The mature form of Mms6 protein used in this study was expressed with a poly(histidine) tag (His-tag) on its N-terminal end. 20,21 Histagged m2Mms6 was generated by shuffling the hydroxyl/carboxyl containing amino acid residues in the C-terminal domain of His-tagged Mms6, such that m2Mms6 shares the same hydropathy profile as Mms6.…”

Section: ■ Introductionmentioning

confidence: 99%

Morphological Transformations in the Magnetite Biomineralizing Protein Mms6 in Iron Solutions: A Small-Angle X-ray Scattering Study

et al. 2015

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Magnetotactic bacteria that produce magnetic nanocrystals of uniform size and well-defined morphologies have inspired the use of biomineralization protein Mms6 to promote formation of uniform magnetic nanocrystals in vitro. Small angle X-ray scattering (SAXS) studies in physiological solutions reveal that Mms6 forms compact globular three-dimensional (3D) micelles (approximately 10 nm in diameter) that are, to a large extent, independent of concentration. In the presence of iron ions in the solutions, the general micellar morphology is preserved, however, with associations among micelles that are induced by iron ions. Compared with Mms6, the m2Mms6 mutant (with the sequence of hydroxyl/carboxyl containing residues in the Cterminal domain shuffled) exhibits subtle morphological changes in the presence of iron ions in solutions. The analysis of the SAXS data is consistent with a hierarchical core-corona micellar structure similar to that found in amphiphilic polymers. The addition of ferric and ferrous iron ions to the protein solution induces morphological changes in the micellar structure by transforming the 3D micelles into objects of reduced dimensionality of 2, with fractal-like characteristics (including Gaussian-chain-like) or, alternatively, plateletlike structures. Small angle X-ray scattering (SAXS) studies in physiological solutions reveal that Mms6 forms compact globular threedimensional (3D) micelles (approximately 10 nm in diameter) that are, to a large extent, independent of concentration. In the presence of iron ions in the solutions, the general micellar morphology is preserved, however, with associations among micelles that are induced by iron ions. Compared with Mms6, the m2Mms6 mutant (with the sequence of hydroxyl/carboxyl containing residues in the C-terminal domain shuffled) exhibits subtle morphological changes in the presence of iron ions in solutions. The analysis of the SAXS data is consistent with a hierarchical core−corona micellar structure similar to that found in amphiphilic polymers. The addition of ferric and ferrous iron ions to the protein solution induces morphological changes in the micellar structure by transforming the 3D micelles into objects of reduced dimensionality of 2, with fractal-like characteristics (including Gaussian-chain-like) or, alternatively, platelet-like structures.

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“…Sizes of magnetite crystals produced by partial oxidation were slightly smaller (average size of about 20 nm) than those produced by co-precipitation (Amemiya et al, 2007;Arakaki et al, 2010). Both magnetite crystals obtained through co-precipitation and through partial oxidation from aqueous and gel solutions have a morphology described as cuboidal or cubo-octahedral (Amemiya et al, 2007;Arakaki et al, 2010;Galloway et al, 2011;Rawlings et al, 2016). Furthermore, magnetite (1 1 1) and (1 0 0) crystal faces were also formed, resembling the truncated crystals produced naturally by Magnetospirillum magneticum AMB-1 (Ameniya et al, 2007;Arakaki et al, 2010).…”

Section: Mms6mentioning

confidence: 98%

“…Uniform magnetite nanocrystals of about 30nm with a protein concentration of 5.6 µg/mL have been obtained through co-precipitation experiments (Prozorov et al, 2007;Galloway et al, 2011;Wang et al, 2012). Compared to those formed in inorganic protein-free experiments, protein-bearing particles were bigger and with a narrower size distribution.…”

Section: Mms6mentioning

confidence: 99%

Magnetita biomimética mediada por proteínas del magnetosoma vs. magnetita del meteorito ALH84001: ¿Son ambas comparables?

Barry-Sosa

Jiménez-López

2016

Fís. Tierra

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The suggestion in 1996 that the Martian meteorite ALH84001 could contain proof of possible biologic activity in the past have generated a huge controversy that last until today. One of the most discussed evidence is the presence of magnetite crystals that resemble those produced by a particular group of bacteria, the so called magnetotactic bacteria (MTB). These microorganisms are the only known example of biologically controlled biomineralization among the prokaryotes and exert an exquisite control over the biomineralization process of intracellular magnetite that result in crystals with very unique features that, so far, cannot be replicated by inorganic means. These unique features have been used to recognize the biological origin of natural terrestrial magnetites, but the problem arises when those same biogenecity criteria are applied to extraterrestrial magnetites. Most of the problems are caused by the fact that it is not clear whether or not some of those characteristics can be reproduced inorganically. Magnetosome protein mediated magnetite synthesis seems to be the best approach to obtain magnetosome-like magnetites, and such strategy may help clarify what is the specific biosignature of magnetotactic bacteria. Key words: ALH84001; Magnetite; MPMS (Magnetosome Protein Mediated Synthesis); Magnetotactic bacteria.Magnetita biomimética mediada por proteínas del magnetosoma vs. magnetita del meteorito ALH84001: ¿Son ambas comparables?Resumen La sugerencia en 1996 de que el meteorito marciano ALH84001 pudiese contener pruebas de posible actividad biológica en el pasado ha generado una gran controversia que aún persiste hoy. Una de las evidencias más discutidas es la presencia de cristales de magnetita que se asemejan a aquellos producidos por un grupo particular de bacterias, las bacterias magnetotácticas (MTB). Estos microorganismos son el único ejemplo de mineralización controlado biológicamente conocido entre procariotas y ejerce un control delicado sobre el proceso de biomineralización de la magnetita intracelular que resulta en la formación de cristales con características únicas que, hasta ahora, no han podido ser replicadas por medios inorgánicos. Estas características únicas se han usado para reconocer el origen biológico de magnetitas terrestres naturales, pero el problema aparece cuando los mismos criterios de biogenicidad se aplican a magnetitas extraterrestres. La mayoría de los problemas se deben a que no está claro si alguna de esas características puede ser reproducida inorgánicamente. La síntesis mediada por proteínas del magnetosoma parece ser la mejor aproximación para obtener magnetitas similares a las de los magneto- A. Barry-Sosa, C. Jiménez-LópezBiomimetic magnetite vs.ALH84001 meteorite Física de la Tierra

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Magnetic bacterial protein Mms6 controls morphology, crystallinity and magnetism of cobalt-doped magnetite nanoparticles in vitro

Cited by 62 publications

References 52 publications

Self-assembled MmsF proteinosomes control magnetite nanoparticle formation in vitro

Self-assembled MmsF proteinosomes control magnetite nanoparticle formation in vitro

Morphological Transformations in the Magnetite Biomineralizing Protein Mms6 in Iron Solutions: A Small-Angle X-ray Scattering Study

Magnetita biomimética mediada por proteínas del magnetosoma vs. magnetita del meteorito ALH84001: ¿Son ambas comparables?

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