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Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation.

ABSTRACT: Bacterial magnetosomes are intracellular compartments that house highly ordered magnetite crystals. By using Magnetospirillum sp. AMB-1 as a model system, we show that magnetosome vesicles exist in the absence of magnetite, biomineralization of magnetite proceeds simultaneously in multiple vesicles, and biomineralization proceeds from the same location in each vesicle. The magnetosome-associated protein, MamA, is required for the formation of functional magnetosome vesicles and displays a dynamic subcellular localization throughout the growth cycle of magnetotactic bacteria. Together, these results suggest that the magnetosome precisely coordinates magnetite biomineralization and can serve as a model system for the study of organelle biogenesis in noneukaryotic cells.

SUBMITTER: Komeili A

PROVIDER: S-EPMC374331 | biostudies-literature | 2004 Mar

REPOSITORIES: biostudies-literature

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Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation.

Komeili Arash A Vali Hojatollah H Beveridge Terrance J TJ Newman Dianne K DK

Proceedings of the National Academy of Sciences of the United States of America 20040302 11

Bacterial magnetosomes are intracellular compartments that house highly ordered magnetite crystals. By using Magnetospirillum sp. AMB-1 as a model system, we show that magnetosome vesicles exist in the absence of magnetite, biomineralization of magnetite proceeds simultaneously in multiple vesicles, and biomineralization proceeds from the same location in each vesicle. The magnetosome-associated protein, MamA, is required for the formation of functional magnetosome vesicles and displays a dynami ...[more]

PMID: 15004275

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Project description:Magnetospirillum gryphiswaldense and related magnetotactic bacteria form magnetosomes, which are membrane-enclosed organelles containing crystals of magnetite (Fe3O4) that cause the cells to orient in magnetic fields. The characteristic sizes, morphologies, and patterns of alignment of magnetite crystals are controlled by vesicles formed of the magnetosome membrane (MM), which contains a number of specific proteins whose precise roles in magnetosome formation have remained largely elusive. Here, we report on a functional analysis of the small hydrophobic MamGFDC proteins, which altogether account for nearly 35% of all proteins associated with the MM. Although their high levels of abundance and conservation among magnetotactic bacteria had suggested a major role in magnetosome formation, we found that the MamGFDC proteins are not essential for biomineralization, as the deletion of neither mamC, encoding the most abundant magnetosome protein, nor the entire mamGFDC operon abolished the formation of magnetite crystals. However, cells lacking mamGFDC produced crystals that were only 75% of the wild-type size and were less regular than wild-type crystals with respect to morphology and chain-like organization. The inhibition of crystal formation could not be eliminated by increased iron concentrations. The growth of mutant crystals apparently was not spatially constrained by the sizes of MM vesicles, as cells lacking mamGFDC formed vesicles with sizes and shapes nearly identical to those formed by wild-type cells. However, the formation of wild-type-size magnetite crystals could be gradually restored by in-trans complementation with one, two, and three genes of the mamGFDC operon, regardless of the combination, whereas the expression of all four genes resulted in crystals exceeding the wild-type size. Our data suggest that the MamGFDC proteins have partially redundant functions and, in a cumulative manner, control the growth of magnetite crystals by an as-yet-unknown mechanism.

Project description:To navigate along the earth's magnetic field, magnetotactic bacteria (MTB) biomineralize iron in unique organelles, the magnetosomes, which are highly ordered, membrane-enclosed, nano-sized crystals of magnetite or greigite1. Magnetosome biogenesis was recently found to be controlled by a large set of genes clustered within a genomic magnetosome island. The unprecedented structural and magnetic properties of magnetosomes and the difficulties to cultivate and manipulate the fastidious bacteria have stimulated ideas to express the underlying biosynthesis pathway in more amenable hosts. However, this has remained an unsolved challenge, owing to the structural complexity of the magnetosome organelle, the insufficient knowledge of involved gene functions, and the challenge to balance expression of numerous proteins. Here we show that the entire gene set required for magnetosome biogenesis can be functionally expressed in the model organism Rhodospirillum rubrum, thereby converting it into a synthetic magnetotactic and phototrophic bacterium. Modular transfer of various cassettes comprising the 30 mam and mms genes that were stitched together by recombinogenic cloning was required and sufficient for biogenesis of magnetosome chains in R. rubrum. However, further auxiliary functions encoded outside these clusters were necessary for biosynthesis of fully developed magnetosomes. Our results for the first time demonstrate that the synthesis of one of the most complex prokaryotic structures can be fully reconstituted within a foreign, hitherto nonmagnetic host. We provide first experimental evidence that the magnetotactic trait can be transmitted horizontally to different species by single or few events of transfer. Conceivably, our findings may enable future synthetic biology approaches for the endogenous production of tailored magnetic nanoparticles within both prokaryotic and eukaryotic organisms, which will be useful for various biotechnological and biomedical applications. Spectra were analyzed via MascotTM software using the NCBI nr Protein Database and a database from M. gryphiswaldense (Richter et al., 2007). Database : Proteindatabase from Richter et al. 2007. Enzyme : Trypsin/P. Fixed modifications : Carbamidomethyl (C). Variable modifications : Oxidation (M). Mass values : Monoisotopic. Protein Mass : Unrestricted. Peptide Mass Tolerance : +/- 10 ppm. Fragment Mass Tolerance: +/- 0.8 Da. Max Missed Cleavages : 2. Instrument type : Default. Number of queries : 4310. Database : NCBInr 201102 (13043846 sequences; 4463804608 residues). Taxonomy : Other Proteobacteria (1938652 sequences). Mascot Version: 2.3.02.

Project description: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.Magnetotactic bacteria synthesize magnetite (Fe3O4) 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.

Dataset Information

Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation.

Publications

Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation.

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