The magnetosome model: insights into the mechanisms of bacterial biomineralization

Rahn-Lee, Lilah; Komeili, Arash

doi:10.3389/fmicb.2013.00352

Cited by 49 publications

(35 citation statements)

References 60 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…mutant of M. gryphiswaldense continued to biomineralize particles of magnetite. Potentially this might be due to unchecked mineral growth after deletion of a major redox regulator (49) and/or the ability of other magnetochrome proteins, like MamX, -E, and -T, to partially compensate the loss of MamP.…”

Section: Discussionmentioning

confidence: 99%

Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense

et al. 2014

View full text Add to dashboard Cite

c Biosynthesis of bacterial magnetosomes, which are intracellular membrane-enclosed, nanosized magnetic crystals, is controlled by a set of >30 specific genes. In Magnetospirillum gryphiswaldense, these are clustered mostly within a large conserved genomic magnetosome island (MAI) comprising the mms6, mamGFDC, mamAB, and mamXY operons. Here, we demonstrate that the five previously uncharacterized genes of the mms6 operon have crucial functions in the regulation of magnetosome biomineralization that partially overlap MamF and other proteins encoded by the adjacent mamGFDC operon. While all other deletions resulted in size reduction, elimination of either mms36 or mms48 caused the synthesis of magnetite crystals larger than those in the wild type (WT). Whereas the mms6 operon encodes accessory factors for crystal maturation, the large mamAB operon contains several essential and nonessential genes involved in various other steps of magnetosome biosynthesis, as shown by single deletions of all mamAB genes. While single deletions of mamL, -P, -Q, -R, -B, -S, -T, and -U showed phenotypes similar to those of their orthologs in a previous study in the related M. magneticum, we found mamI and mamN to be not required for at least rudimentary iron biomineralization in M. gryphiswaldense. Thus, only mamE, -L, -M, -O, -Q, and -B were essential for formation of magnetite, whereas a mamI mutant still biomineralized tiny particles which, however, consisted of the nonmagnetic iron oxide hematite, as shown by high-resolution transmission electron microscopy (HRTEM) and the X-ray absorption near-edge structure (XANES). Based on this and previous studies, we propose an extended model for magnetosome biosynthesis in M. gryphiswaldense. Magnetotactic bacteria (MTB) orient along Earth's magnetic field lines to navigate to their growth-favoring microoxic habitats within stratified aquatic sediments (1). This behavior is enabled by the synthesis of ferrimagnetic intracellular organelles termed magnetosomes (2). In the alphaproteobacterium Magnetospirillum gryphiswaldense and related MTB, magnetosomes consist of crystals of the magnetic iron oxide magnetite (Fe 3 O 4 ) enclosed by the magnetosome membrane (MM), which contains a specific set of about 30 proteins (3, 4). The biosynthesis of magnetosomes is a complex process that comprises the (i) invagination of vesicles from the inner membrane (5, 6), (ii) sorting of magnetosome proteins to the MM (7), (iii) iron transport and crystallization of magnetite crystals (8), (iv) crystal maturation (7), and (v) assembly as well as positioning of mature crystals into a linear chain along a filamentous cytoskeletal structure (6, 9). Each step is under strict genetic control, and responsible genes were found to be located mostly within a genomic magnetosome island (MAI) (10, 11), comprising the mms6 operon (mms6 op ), mamGFDC operon (mamGFDC op ), mamAB operon (mamAB op ), and mamXY operon (mamXY op ) (10-12). These operons were found to be highly conserved also in the closely related Magnetospiri...

show abstract

Section: Discussionmentioning

confidence: 99%

Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense

et al. 2014

View full text Add to dashboard Cite

show abstract

“…The Mms6 gene translation product is predicted as a transmembrane protein and the transmembrane helix contains only hydrophobic residues. 45 The ODT surface may create conditions for the protein that are more similar to its native lipid bilayer environment of magnetosome membrane, thus facilitating the formation of uniformly sized and more well-defined magnetite nanoparticles, 46 similar to those seen in nature.…”

Section: Industrial and Engineering Chemistry Researchmentioning

confidence: 99%

Effect of Surface Hydrophobicity on the Function of the Immobilized Biomineralization Protein Mms6

Liu

Zhang

Nayak

et al. 2015

Ind. Eng. Chem. Res.

View full text Add to dashboard Cite

Magnetotactic bacteria produce magnetic nanocrystals with uniform shapes and sizes in nature, which has inspired in vitro synthesis of uniformly sized magnetite nanocrystals under mild conditions. Mms6, a biomineralization protein from magnetotactic bacteria with a hydrophobic N-terminal domain and a hydrophilic C-terminal domain, can promote formation of magnetite nanocrystals in vitro with well-defined shape and size in gels under mild conditions. Here we investigate the role of surface hydrophobicity on the ability of Mms6 to template magnetite nanoparticle formation on surfaces. Our results confirmed that Mms6 can form a protein network structure on a monolayer of hydrophobic octadecanethiol (ODT)-coated gold surfaces and facilitate magnetite nanocrystal formation with uniform sizes close to those seen in nature, in contrast to its behavior on more hydrophilic surfaces. We propose that this hydrophobicity effect might be due to the amphiphilic nature of the Mms6 protein and its tendency to incorporate the hydrophobic Nterminal domain into the hydrophobic lipid bilayer environment of the magnetosome membrane, exposing the hydrophilic C-terminal domain that promotes biomineralization. Supporting this hypothesis, the larger and well-formed magnetite nanoparticles were found to be preferentially located on ODT surfaces covered with Mms6 as compared to control samples, as characterized by scanning electron microscopy, X-ray diffraction, X-ray photoelectron spectroscopy, and atomic force microscopy studies. A C-terminal domain mutant of this protein did not form the same network structure as wild-type Mms6, suggesting that the network structure is important for the magnetite nanocrystal formation. This study provides valuable insights into the role of surface hydrophilicity on the action of the biomineralization protein Mms6 to synthesize magnetic nanocrystals and provides a facile route to controlling bioinspired nanocrystal synthesis in vitro. ABSTRACT: Magnetotactic bacteria produce magnetic nanocrystals with uniform shapes and sizes in nature, which has inspired in vitro synthesis of uniformly sized magnetite nanocrystals under mild conditions. Mms6, a biomineralization protein from magnetotactic bacteria with a hydrophobic N-terminal domain and a hydrophilic C-terminal domain, can promote formation of magnetite nanocrystals in vitro with well-defined shape and size in gels under mild conditions. Here we investigate the role of surface hydrophobicity on the ability of Mms6 to template magnetite nanoparticle formation on surfaces. Our results confirmed that Mms6 can form a protein network structure on a monolayer of hydrophobic octadecanethiol (ODT)-coated gold surfaces and facilitate magnetite nanocrystal formation with uniform sizes close to those seen in nature, in contrast to its behavior on more hydrophilic surfaces. We propose that this hydrophobicity effect might be due to the amphiphilic nature of the Mms6 protein and its tendency to incorporate the hydrophobic N-terminal domain into the hydroph...

show abstract

“…The crystal sizes and shapes are highly regulated, and Ͼ10 magnetosomes typically align along the cell's long axis (8)(9)(10). Thus, the formation of magnetosomes confers a magnetic moment to the cells and allows them to migrate along oxygen gradients in an aquatic environment under the influence of the Earth's geomagnetic field (7).…”

mentioning

confidence: 99%

Comparative Subcellular Localization Analysis of Magnetosome Proteins Reveals a Unique Localization Behavior of Mms6 Protein onto Magnetite Crystals

et al. 2016

View full text Add to dashboard Cite

The magnetosome is an organelle specialized for inorganic magnetite crystal synthesis in magnetotactic bacteria. The complex mechanism of magnetosome formation is regulated by magnetosome proteins in a stepwise manner. Protein localization is a key step for magnetosome development; however, a global study of magnetosome protein localization remains to be conducted. Here, we comparatively analyzed the subcellular localization of a series of green fluorescent protein (GFP)-tagged magnetosome proteins. The protein localizations were categorized into 5 groups (short-length linear, middle-length linear, long-length linear, cell membrane, and intracellular dispersing), which were related to the protein functions. Mms6, which regulates magnetite crystal growth, localized along magnetosome chain structures under magnetite-forming (microaerobic) conditions but was dispersed in the cell under nonforming (aerobic) conditions. Correlative fluorescence and electron microscopy analyses revealed that Mms6 preferentially localized to magnetosomes enclosing magnetite crystals. We suggest that a highly organized spatial regulation mechanism controls magnetosome protein localization during magnetosome formation in magnetotactic bacteria. IMPORTANCEMagnetotactic bacteria synthesize magnetite (Fe 3 O 4 ) nanocrystals in a prokaryotic organelle called the magnetosome. This organelle is formed using various magnetosome proteins in multiple steps, including vesicle formation, magnetosome alignment, and magnetite crystal formation, to provide compartmentalized nanospaces for the regulation of iron concentrations and redox conditions, enabling the synthesis of a morphologically controlled magnetite crystal. Thus, to rationalize the complex organelle development, the localization of magnetosome proteins is considered to be highly regulated; however, the mechanisms remain largely unknown. Here, we performed comparative localization analysis of magnetosome proteins that revealed the presence of a spatial regulation mechanism within the linear structure of magnetosomes. This discovery provides evidence of a highly regulated protein localization mechanism for this bacterial organelle development. P rotein localization at appropriate positions within a cell is an essential mechanism for the effective performance of the diverse biological reactions that occur within the restricted intracellular area in both eukaryotes and prokaryotes. In various prokaryotes, intracellular compartments can be created to provide the domains required for highly specialized reactions. Whereas some of these compartments are completely proteinaceous (e.g., carboxysomes, metabolosomes, and ferritin) (1-3), others contain molecular components similar to those in cell membranes, including lipids and proteins (e.g., nucleoids, polyhydroxybutyrate, and spores) (4, 5). Such compartmentalized organelles are recognized to be formed within bacteria through multiple processes involving the spatial regulation of protein localization, but the details of this regulatory m...

show abstract

The magnetosome model: insights into the mechanisms of bacterial biomineralization

Cited by 49 publications

References 60 publications

Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense

Genetic Dissection of the mamAB and mms6 Operons Reveals a Gene Set Essential for Magnetosome Biogenesis in Magnetospirillum gryphiswaldense

Effect of Surface Hydrophobicity on the Function of the Immobilized Biomineralization Protein Mms6

Comparative Subcellular Localization Analysis of Magnetosome Proteins Reveals a Unique Localization Behavior of Mms6 Protein onto Magnetite Crystals

Contact Info

Product

Resources

About