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Journal of Bacteriology Jun 2024Magnetotactic bacteria are a diverse group of microbes that use magnetic particles housed within intracellular lipid-bounded magnetosome organelles to guide navigation...
Magnetotactic bacteria are a diverse group of microbes that use magnetic particles housed within intracellular lipid-bounded magnetosome organelles to guide navigation along geomagnetic fields. The development of magnetosomes and their magnetic crystals in AMB-1 requires the coordinated action of numerous proteins. Most proteins are thought to localize to magnetosomes during the initial stages of organelle biogenesis, regardless of environmental conditions. However, the magnetite-shaping protein Mms6 is only found in magnetosomes that contain magnetic particles, suggesting that it might conditionally localize after the formation of magnetosome membranes. The mechanisms for this unusual mode of localization to magnetosomes are unclear. Here, using pulse-chase labeling, we show that Mms6 translated under non-biomineralization conditions translocates to pre-formed magnetosomes when cells are shifted to biomineralizing conditions. Genes essential for magnetite production, namely and are necessary for Mms6 localization, whereas inhibits Mms6 localization. MamD localization was also investigated and found to be controlled by similar cellular factors. The membrane localization of Mms6 is dependent on a glycine-leucine repeat region, while the N-terminal domain of Mms6 is necessary for retention in the cytosol and impacts conditional localization to magnetosomes. The N-terminal domain is also sufficient to impart conditional magnetosome localization to MmsF, altering its native constitutive magnetosome localization. Our work illuminates an alternative mode of protein localization to magnetosomes in which Mms6 and MamD are excluded from magnetosomes by MamN until biomineralization initiates, whereupon they translocate into magnetosome membranes to control the development of growing magnetite crystals.IMPORTANCEMagnetotactic bacteria (MTB) are a diverse group of bacteria that form magnetic nanoparticles surrounded by membranous organelles. MTB are widespread and serve as a model for bacterial organelle formation and biomineralization. Magnetosomes require a specific cohort of proteins to enable magnetite formation, but how those proteins are localized to magnetosome membranes is unclear. Here, we investigate protein localization using pulse-chase microscopy and find a system of protein coordination dependent on biomineralization-permissible conditions. In addition, our findings highlight a protein domain that alters the localization behavior of magnetosome proteins. Utilization of this protein domain may provide a synthetic route for conditional functionalization of magnetosomes for biotechnological applications.
Topics: Magnetospirillum; Magnetosomes; Bacterial Proteins; Gene Expression Regulation, Bacterial; Protein Transport
PubMed: 38819153
DOI: 10.1128/jb.00008-24 -
Advanced Science (Weinheim,... Oct 2022Metal sulfides are a common group of extracellular bacterial biominerals. However, only a few cases of intracellular biomineralization are reported in this group, mostly...
Metal sulfides are a common group of extracellular bacterial biominerals. However, only a few cases of intracellular biomineralization are reported in this group, mostly limited to greigite (Fe S ) in magnetotactic bacteria. Here, a previously unknown periplasmic biomineralization of copper sulfide produced by the magnetotactic bacterium Desulfamplus magnetovallimortis strain BW-1, a species known to mineralize greigite (Fe S ) and magnetite (Fe O ) in the cytoplasm is reported. BW-1 produces hundreds of spherical nanoparticles, composed of 1-2 nm substructures of a poorly crystalline hexagonal copper sulfide structure that remains in a thermodynamically unstable state. The particles appear to be surrounded by an organic matrix as found from staining and electron microscopy inspection. Differential proteomics suggests that periplasmic proteins, such as a DegP-like protein and a heavy metal-binding protein, could be involved in this biomineralization process. The unexpected periplasmic formation of copper sulfide nanoparticles in BW-1 reveals previously unknown possibilities for intracellular biomineralization that involves intriguing biological control and holds promise for biological metal recovery in times of copper shortage.
Topics: Bacteria; Biomineralization; Copper; Ferrosoferric Oxide; Iron; Magnetosomes; Nanoparticles; Periplasmic Proteins; Sulfides
PubMed: 35975419
DOI: 10.1002/advs.202203444 -
Frontiers in Microbiology 2021Magnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (FeO), and/or greigite (FeS) crystals in intracellular...
Magnetotactic bacteria (MTB) are a group of microbes that biomineralize membrane-bound, nanosized magnetite (FeO), and/or greigite (FeS) crystals in intracellular magnetic organelle magnetosomes. MTB belonging to the phylum can form up to several hundreds of FeO magnetosome crystals and dozens of sulfur globules in a single cell. These MTB are widespread in aquatic environments and sometimes account for a significant proportion of microbial biomass near the oxycline, linking these lineages to the key steps of global iron and sulfur cycling. Despite their ecological and biogeochemical importance, our understanding of the diversity and ecophysiology of magnetotactic is still very limited because this group of MTB remains unculturable. Here, we identify and characterize two previously unknown MTB populations within the phylum through a combination of 16S rRNA gene-based and genome-resolved metagenomic analyses. These two MTB populations represent distinct morphotypes (rod-shaped and coccoid, designated as XYR, and XYC, respectively), and both form more than 100 bullet-shaped magnetosomal crystals per cell. High-quality draft genomes of XYR and XYC have been reconstructed, and they represent a novel species and a novel genus, respectively, according to their average amino-acid identity values with respect to available genomes. Accordingly, the names Magnetobacterium cryptolimnobacter and Magnetomicrobium cryptolimnococcus for XYR and XYC, respectively, were proposed. Further comparative genomic analyses of XYR, XYC, and previously reported magnetotactic reveal the general metabolic potential of this MTB group in distinct microenvironments, including CO fixation, dissimilatory sulfate reduction, sulfide oxidation, nitrogen fixation, or denitrification processes. A remarkably conserved magnetosome gene cluster has been identified across MTB genomes, indicating its putative important adaptive roles in these bacteria. Taken together, the present study provides novel insights into the phylogenomic diversity and ecophysiology of this intriguing, yet poorly understood MTB group.
PubMed: 34385986
DOI: 10.3389/fmicb.2021.690052 -
RSC Advances Nov 2022Metal oxide nanoparticles have attracted increased attention due to their emerging applications in cancer detection and therapy. This study envisioned to highlight the... (Review)
Review
Metal oxide nanoparticles have attracted increased attention due to their emerging applications in cancer detection and therapy. This study envisioned to highlight the great potential of metal oxide NPs due to their interesting properties including high payload, response to magnetic field, affluence of surface modification to overcome biological barriers, and biocompatibility. Mammogram, ultrasound, X-ray computed tomography (CT), MRI, positron emission tomography (PET), optical or fluorescence imaging are used for breast imaging. Drug-loaded metal oxide nanoparticle delivered to the breast cancer cells leads to higher drug uptake. Thus, enhanced the cytotoxicity to target cells compared to free drug. The drug loaded metal oxide nanoparticle formulations hold great promise to enhance efficacy of breast cancer therapy including multidrug resistant (MDR) and metastatic breast cancers. Various metal oxides including magnetic metal oxides and magnetosomes are of current interests to explore cancer drug delivery and diagnostic efficacy especially for metastatic breast cancer. Metal oxide-based nanocarrier formulations are promising for their usage in drug delivery and release to breast cancer cells, cancer diagnosis and their clinical translations.
PubMed: 36425155
DOI: 10.1039/d2ra02005j -
Nature Communications Sep 2022Magnetotactic bacteria are a diverse group of microorganisms that use intracellular chains of ferrimagnetic nanocrystals, produced within magnetosome organelles, to...
Magnetotactic bacteria are a diverse group of microorganisms that use intracellular chains of ferrimagnetic nanocrystals, produced within magnetosome organelles, to align and navigate along the geomagnetic field. Several conserved genes for magnetosome formation have been described, but the mechanisms leading to distinct species-specific magnetosome chain configurations remain unclear. Here, we show that the fragmented nature of magnetosome chains in Magnetospirillum magneticum AMB-1 is controlled by genes mcaA and mcaB. McaA recognizes the positive curvature of the inner cell membrane, while McaB localizes to magnetosomes. Along with the MamK actin-like cytoskeleton, McaA and McaB create space for addition of new magnetosomes in between pre-existing magnetosomes. Phylogenetic analyses suggest that McaA and McaB homologs are widespread among magnetotactic bacteria and may represent an ancient strategy for magnetosome positioning.
Topics: Actins; Bacterial Proteins; Magnetic Phenomena; Magnetosomes; Magnetospirillum; Phylogeny
PubMed: 36163114
DOI: 10.1038/s41467-022-32914-9 -
Bioengineered Jan 2018The need for cost-effectively produced and improved biocatalysts for industrial, pharmaceutical and environmental processes is steadily increasing. While enzyme... (Review)
Review
The need for cost-effectively produced and improved biocatalysts for industrial, pharmaceutical and environmental processes is steadily increasing. While enzyme properties themselves can be improved via protein engineering, immobilization by attachment to carrier materials remains a critical step for stabilization and process implementation. A new emerging immobilization approach, the in situ immobilization, enables simultaneous production of highly active enzymes and carrier materials using bioengineering/synthetic biology of microbial cells. In situ enzyme immobilization holds the promise of cost-effective production of highly functional immobilized biocatalysts for uses such as in bioremediation, drug synthesis, bioenergy and food processing.
Topics: Adsorption; Biocatalysis; Biodegradation, Environmental; Cross-Linking Reagents; Enzymes, Immobilized; Food Handling; Gene Expression; Inclusion Bodies; Magnetosomes; Polyhydroxyalkanoates; Protein Engineering; Proteolipids; Recombinant Fusion Proteins
PubMed: 28463573
DOI: 10.1080/21655979.2017.1325040 -
Journal of Structural Biology: X 2021Biomineralization is the process of mineral formation by living organisms. One notable example of these organisms is magnetotactic bacteria (MTB). MTB are Gram-negative... (Review)
Review
Biomineralization is the process of mineral formation by living organisms. One notable example of these organisms is magnetotactic bacteria (MTB). MTB are Gram-negative bacteria that can biomineralize iron into magnetic nanoparticles. This ability allows these aquatic microorganisms to orient themselves according to the geomagnetic field. The biomineralization process takes place in a specialized sub-cellular membranous organelle, the magnetosome. The magnetosome contains a defined set of magnetosome-associated proteins (MAPs) that controls the biomineralization environment, including iron concentration, redox, and pH. Magnetite formation is subjected to a tight regulation within the magnetosome that affects the nanoparticle nucleation, size, and shape, leading to well-defined magnetic properties. The formed magnetite nanoparticles have unique characteristics of a stable, single magnetic domain with narrow size distribution and high crystalline structures, which turned MTB into the subject of interest in multidisciplinary research. This graphical review provides a current overview of iron biomineralization in magnetotactic bacteria, focusing on Alphaproteobacteria. To better understand this complex mechanism, we present the four main steps and the main MAPs participating in the process of magnetosome formation.
PubMed: 34723168
DOI: 10.1016/j.yjsbx.2021.100052 -
Frontiers in Microbiology Nov 2013Though the most ready example of biomineralization is the calcium phosphate of vertebrate bones and teeth, many bacteria are capable of creating biominerals inside their... (Review)
Review
Though the most ready example of biomineralization is the calcium phosphate of vertebrate bones and teeth, many bacteria are capable of creating biominerals inside their cells. Because of the diversity of these organisms and the minerals they produce, their study may reveal aspects of the fundamental mechanisms of biomineralization in more complex organisms. The best-studied case of intracellular biomineralization in bacteria is the magnetosome, an organelle produced by a diverse group of aquatic bacteria that contains single-domain crystals of the iron oxide magnetite (Fe3O4) or the iron sulfide greigite (Fe3S4). Here, recent advances in our understanding of the mechanisms of bacterial magnetite biomineralization are discussed and used as a framework for understanding less-well studied examples, including the bacterial intracellular biomineralization of cadmium, selenium, silver, nickel, uranium, and calcium carbonate. Understanding the molecular mechanisms underlying the biological formation of these minerals will have important implications for technologies such as the fabrication of nanomaterials and the bioremediation of toxic compounds.
PubMed: 24324464
DOI: 10.3389/fmicb.2013.00352 -
Proceedings of the National Academy of... Feb 2017Microbes that synthesize minerals, a process known as microbial biomineralization, contributed substantially to the evolution of current planetary environments through...
Microbes that synthesize minerals, a process known as microbial biomineralization, contributed substantially to the evolution of current planetary environments through numerous important geochemical processes. Despite its geological significance, the origin and evolution of microbial biomineralization remain poorly understood. Through combined metagenomic and phylogenetic analyses of deep-branching magnetotactic bacteria from the phylum, and using a Bayesian molecular clock-dating method, we show here that the gene cluster responsible for biomineralization of magnetosomes, and the arrangement of magnetosome chain(s) within cells, both originated before or near the Archean divergence between the and This phylogenetic divergence occurred well before the Great Oxygenation Event. Magnetotaxis likely evolved due to environmental pressures conferring an evolutionary advantage to navigation via the geomagnetic field. Earth's dynamo must therefore have been sufficiently strong to sustain microbial magnetotaxis in the Archean, suggesting that magnetotaxis coevolved with the geodynamo over geological time.
Topics: Bacterial Proteins; Bayes Theorem; Biological Evolution; Gene Expression; Genome, Bacterial; Magnetic Fields; Magnetosomes; Phylogeny; Proteobacteria; Taxis Response
PubMed: 28193877
DOI: 10.1073/pnas.1614654114 -
Scientific Reports May 2016Polyhydroxybutyrate (PHB) granules, also designated as carbonosomes, are supra-molecular complexes in prokaryotes consisting of a PHB polymer core and a surface layer of...
Polyhydroxybutyrate (PHB) granules, also designated as carbonosomes, are supra-molecular complexes in prokaryotes consisting of a PHB polymer core and a surface layer of structural and functional proteins. The presence of suspected phospholipids in the surface layer is based on in vitro data of isolated PHB granules and is often shown in cartoons of the PHB granule structure in reviews on PHB metabolism. However, the in vivo presence of a phospholipid layer has never been demonstrated. We addressed this topic by the expression of fusion proteins of DsRed2EC and other fluorescent proteins with the phospholipid-binding domain (LactC2) of lactadherin in three model organisms. The fusion proteins specifically localized at the cell membrane of Ralstonia eutropha but did not co-localize with PHB granules. The same result was obtained for Pseudomonas putida, a species that accumulates another type of polyhydroxyalkanoate (PHA) granules related to PHB. Notably, DsRed2EC-LactC2 expressed in Magnetospirillum gryphiswaldense was detected at the position of membrane-enclosed magnetosome chains and at the cytoplasmic membrane but not at PHB granules. In conclusion, the carbonosomes of representatives of α-proteobacteria, β-proteobacteria and γ-proteobacteria have no phospholipids in vivo and we postulate that the PHB/PHA granule surface layers in natural producers generally are free of phospholipids and consist of proteins only.
Topics: Bacteria; Cytoplasmic Granules; Phospholipids; Polyhydroxyalkanoates
PubMed: 27222167
DOI: 10.1038/srep26612