mamO and mamE genes are essential for magnetosome crystal biomineralization in Magnetospirillum gryphiswaldense MSR-1

Yang, Wei; Li, Ruiguo; Peng, Tao; Zhang, Yang; Jiang, Wei; Li, Ying; Li, Jilun

doi:10.1016/j.resmic.2010.07.002

Cited by 42 publications

(53 citation statements)

References 17 publications

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“…In addition to the previously identified mamE (34), mamM (35), mamO (34), and mamB (35) genes, we also demonstrated mamQ and most probably mamL to be essential genes for magnetosome synthesis in M. gryphiswaldense, since their deletions abolished the biomineralization of clearly distinguishable electron-dense particles. MamQ (23).…”

Section: Discussionsupporting

confidence: 75%

“…However, this ability of MamP is not essential in vivo, as the ⌬mamP (18,22). Red arrows, genes essential for magnetosome crystal formation; blue arrows, genes nonessential for particle formation; gray bars, nonessential genes for which deletion strains were previously generated (6,9,20); blue bars, nonessential genes for which deletions were generated in this study; dark red bars, essential genes for which deletions were generated previously (34,35); light red bars, essential genes for which deletions were generated in this study; white arrows, magnetosome chains or particles; black arrows, PHB granules. mutant of M. gryphiswaldense continued to biomineralize particles of magnetite.…”

Section: Discussionmentioning

confidence: 75%

“…Deletion of mamH caused a moderate decrease of magnetosome number and size, whereas codeletion of mamH and its partial homolog mamZ had a considerably stronger effect, with only very few or no regular crystals detectable in the cells (20). Deletion of mamE, -O, -M, and -B either resulted in a total inhibition of crystal nucleation or prevented MM vesicle synthesis (18,34,35). However, mamI, -L, -N, -P, -A, -Q, -R, -S, -T, and -U have not yet been analyzed individually by mutagenesis, and it has remained unknown whether they have functions similar to or distinct from those of their corresponding orthologs in M. magneticum.…”

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confidence: 99%

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

et al. 2014

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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...

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Section: Discussionsupporting

confidence: 75%

Section: Discussionmentioning

confidence: 75%

mentioning

confidence: 99%

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

et al. 2014

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“…Nevertheless, the transcomplemented mutant still showed a survival rate lower than that of the WT. However, an intermediate rate of transcomplementation was also shown for other genes of M. gryphiswaldense (31,46). Most notably, homologous recombination was decreased 80-fold in IK-1.…”

Section: Discussionmentioning

confidence: 71%

Frequent Mutations within the Genomic Magnetosome Island of Magnetospirillum gryphiswaldense Are Mediated by RecA

et al. 2011

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Genes for magnetosome formation in magnetotactic bacteria are clustered in large genomic magnetosome islands (MAI). Spontaneous deletions and rearrangements were frequently observed within these regions upon metabolic stress. This instability was speculated to be due to RecA-dependent homologous recombination between the numerous sequence repeats present within the MAI. Here we show that a RecA-deficient strain of Magnetospirillum gryphiswaldense (IK-1) no longer exhibits genetic instability of magnetosome formation. Strain IK-1 displayed higher sensitivity to oxygen and UV irradiation. Furthermore, the lack of RecA abolished allelic exchange in the mutant. Cells of strain IK-1 displayed a slightly altered (i.e., more elongated) morphology, whereas the absence of RecA did not affect the ability to synthesize wild-type-like magnetosomes. Our data provide evidence that the observed genetic instability of magnetosome formation in the wild type is due predominantly to RecA-mediated recombination. In addition, increased genetic stability could make strain IK-1 a useful tool for the expression of genes and further genetic engineering, as well as for biotechnological production of bacterial magnetosomes.

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“…Because it has higher similarity to the C terminus of MamO (TauE domain), we annotated this gene as mamOCter gene (Figure 4). Both MamO and MamE are predicted as serine proteases, and are likely involved in magnetosome protein localization, biomineralization activation and crystal maturation as demonstrated in Magnetospirillum strains of the Alphaproteobacteria (Murat et al, 2010;Yang et al, 2010;Komeili, 2012).…”

Section: Magnetosome Biomineralizationmentioning

confidence: 99%

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

et al. 2014

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Magnetotactic bacteria (MTB) of the genus 'Candidatus Magnetobacterium' in phylum Nitrospirae are of great interest because of the formation of hundreds of bullet-shaped magnetite magnetosomes in multiple bundles of chains per cell. These bacteria are worldwide distributed in aquatic environments and have important roles in the biogeochemical cycles of iron and sulfur. However, except for a few short genomic fragments, no genome data are available for this ecologically important genus, and little is known about their metabolic capacity owing to the lack of pure cultures. Here we report the first draft genome sequence of 3.42 Mb from an uncultivated strain tentatively named 'Ca. Magnetobacterium casensis' isolated from Lake Miyun, China. The genome sequence indicates an autotrophic lifestyle using the Wood-Ljungdahl pathway for CO 2 fixation, which has not been described in any previously known MTB or Nitrospirae organisms. Pathways involved in the denitrification, sulfur oxidation and sulfate reduction have been predicted, indicating its considerable capacity for adaptation to variable geochemical conditions and roles in local biogeochemical cycles. Moreover, we have identified a complete magnetosome gene island containing mam, mad and a set of novel genes (named as man genes) putatively responsible for the formation of bullet-shaped magnetite magnetosomes and the arrangement of multiple magnetosome chains. This first comprehensive genomic analysis sheds light on the physiology, ecology and biomineralization of the poorly understood 'Ca. Magnetobacterium' genus.

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mamO and mamE genes are essential for magnetosome crystal biomineralization in Magnetospirillum gryphiswaldense MSR-1

Cited by 42 publications

References 17 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

Frequent Mutations within the Genomic Magnetosome Island of Magnetospirillum gryphiswaldense Are Mediated by RecA

Genomic insights into the uncultured genus ‘Candidatus Magnetobacterium’ in the phylum Nitrospirae

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