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

Kolinko, Isabel; Jogler, Christian; Katzmann, Emanuel; Schüler, Dirk

doi:10.1128/jb.05491-11

Cited by 34 publications

(45 citation statements)

References 48 publications

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“…In addition, there was also the possibility of gene loss, for example, the loss of mam genes, which has been shown to occur in cultures of some magnetotactic bacteria that also lost the magnetotactic trait (Ullrich et al, 2005;Kolinko et al, 2011). This unique application of genomic sequencing and analysis of microbial environmental DNA contributed to the understanding of many physiological features involved in the behavior and multicellular life of Ca.…”

Section: Discussionmentioning

confidence: 99%

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

et al. 2013

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Candidatus Magnetoglobus multicellularis (Ca. M. multicellularis) is a member of a group of uncultured magnetotactic prokaryotes that possesses a unique multicellular morphology. To better understand this organism's physiology, we used a genomic approach through pyrosequencing. Genomic data analysis corroborates previous structural studies and reveals the proteins that are likely involved in multicellular morphogenesis of this microorganism. Interestingly, some detected protein sequences that might be involved in cell adhesion are homologues to phylogenetically unrelated filamentous multicellular bacteria proteins, suggesting their contribution in the early development of multicellular organization in Bacteria. Genes related to the behavior of Ca. M. multicellularis (chemo-, photo-and magnetotaxis) and its metabolic capabilities were analyzed. On the basis of the genomic-physiologic information, enrichment media were tested. One medium supported chemoorganoheterotrophic growth of Ca. M. multicellularis and allowed the microorganisms to maintain their multicellular morphology and cell cycle, confirming for the first time that the entire life cycle of the MMP occurs in a multicellular form. Because Ca. M. multicellularis has a unique multicellular life style, its cultivation is an important achievement for further studies regarding the multicellular evolution in prokaryotes.

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Section: Discussionmentioning

confidence: 99%

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

et al. 2013

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“…The applied magnetic field for C mag measurements was about 70 mT, which is able to magnetize very small or irregular magnetosomes within the superparamagnetic state. Intracellular iron concentrations were measured after incubation under anaerobic conditions as described previously (39).…”

Section: Methodsmentioning

confidence: 99%

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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“…Gene rearrangements, gene deletions, and duplications may be the reason for the frequent development of spontaneous nonmagnetotactic mutants of various strains (68,170). Spontaneous deletions that lead to a loss of the magnetotactic phenotype with a frequency of 10 Ϫ2 were observed under starvation condi-tions in late-stationary-phase cultures of Ms. gryphiswaldense and most likely were caused by RecA-dependent homologous recombination between numerous repeats present in the MAI (197,217). Frequent nonmagnetic mutants that do not synthesize magnetosomes were also observed in cultures of Magnetovibrio blakemorei (68) and Ms. magneticum (164,215).…”

Section: Evidence For Hgt Of Magnetosome Genes In Mtbmentioning

confidence: 99%

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

Lefèvre

Bazylinski

2013

Microbiol Mol Biol Rev

376

388

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SUMMARY Magnetotactic bacteria (MTB) are widespread, motile, diverse prokaryotes that biomineralize a unique organelle called the magnetosome. Magnetosomes consist of a nano-sized crystal of a magnetic iron mineral that is enveloped by a lipid bilayer membrane. In cells of almost all MTB, magnetosomes are organized as a well-ordered chain. The magnetosome chain causes the cell to behave like a motile, miniature compass needle where the cell aligns and swims parallel to magnetic field lines. MTB are found in almost all types of aquatic environments, where they can account for an important part of the bacterial biomass. The genes responsible for magnetosome biomineralization are organized as clusters in the genomes of MTB, in some as a magnetosome genomic island. The functions of a number of magnetosome genes and their associated proteins in magnetosome synthesis and construction of the magnetosome chain have now been elucidated. The origin of magnetotaxis appears to be monophyletic; that is, it developed in a common ancestor to all MTB, although horizontal gene transfer of magnetosome genes also appears to play a role in their distribution. The purpose of this review, based on recent progress in this field, is focused on the diversity and the ecology of the MTB and also the evolution and transfer of the molecular determinants involved in magnetosome formation.

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

Cited by 34 publications

References 48 publications

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics

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

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

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