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Introduction
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July 2001 - June 2005
July 2005 - December 2012
September 1996 - June 2001
Education
September 1996 - May 2001
September 1992 - May 1996
Publications
Publications (81)
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 Magnetospirillum magneticum AMB-1 requires the coordinated action of numerous proteins. Most...
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. Development of magnetosomes and their magnetic crystals in Magnetospirillum magneticum AMB-1 requires the coordinated action of numerous proteins. Most prot...
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 magnetosom...
Cellular iron homeostasis is vital and maintained through tight regulation of iron import, efflux, storage and detoxification1–3. The most common modes of iron storage use proteinaceous compartments, such as ferritins and related proteins4,5. Although lipid-bounded iron compartments have also been described, the basis for their formation and functi...
Magnetotactic bacteria (MTB) are a diverse group of microorganisms that use intracellular chains of ferrimagnetic nanocrystals, produced within their magnetosome organelles, to align and navigate along the geomagnetic field. The cell biological and biochemical properties of magnetosomes make them a powerful model for studying the molecular mechanis...
Significance
Biomineralization, the process by which elaborate three-dimensional structures are built out of organic and inorganic molecules, is central to health and survival of many organisms. In some magnetotactic bacteria, the growth of magnetosome membranes is closely correlated to the progression of mineral formation. However, the molecular m...
Magnetotactic bacteria (MTB) are a group of bacteria that can form nano-sized crystals of magnetic minerals. MTB are likely an important part of their ecosystems, because they can account for up to a third of the microbial biomass in an aquatic habitat and consume large amounts of iron, potentially impacting the iron cycle.
Magnetotactic bacteria (MTB) produce single‐stranded or multi‐stranded chains of magnetic nanoparticles that contribute to the magnetization of sediments and rocks. Their magnetic fingerprint can be detected in ancient geological samples and serve as a unique biosignature of microbial life. However, some fossilized assemblages bear contradictory si...
Magnetotactic bacteria (MTB) are a phylogenetically diverse group of bacteria remarkable for their ability to biomineralize magnetite (Fe 3 O 4 ) or greigite (Fe 3 S 4 ) in organelles called magnetosomes. The majority of genes required for magnetosome formation are encoded by a magnetosome gene island (MAI). Here, we conducted random barcoded trans...
Magnetotactic bacteria (MTB) produce single- or multi-stranded chains of magnetic nanoparticles that contribute to the magnetization of sedimentary rocks. Their magnetic fingerprint can be detected in ancient geological samples, and serve as a unique biosignature of microbial life. However, fossilized assemblages bear contradictory signatures point...
Magnetotactic bacteria (MTB) produce iron-based intracellular magnetic crystals. They represent a model system for studying iron homeostasis and biomineralization in microorganisms. MTB sequester a large amount of iron in their crystals and have thus been proposed to significantly impact the iron biogeochemical cycle. Several studies proposed that...
Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that form intracellular nanoparticles of magnetite (Fe 3 O 4 ) or greigite (Fe 3 S 4 ) in a genetically controlled manner. Magnetite and greigite synthesis requires MTB to transport a large amount of iron from the environment which is subsequently concentrated in organelles called m...
Many species of bacteria can manufacture materials on a finer scale than those that are synthetically made. These products are often produced within intracellular compartments that bear many hallmarks of eukaryotic organelles. One unique and elegant group of organisms is at the forefront of studies into the mechanisms of organelle formation and bio...
Cellular iron homeostasis is vital and maintained through tight regulation of iron import, efflux, storage, and detoxification. The most common modes of iron storage employ proteinaceous compartments that are composed of ferritin or related proteins. While lipid-bounded iron compartments have also been described, the basis for their formation and f...
Magnetotactic bacteria (MTB) naturally synthesize magnetic nanoparticles that are wrapped in lipid membranes. These membrane‐bound particles, which are known as magnetosomes, are characterized by their narrow size distribution, high colloidal stability, and homogenous magnetic properties. These characteristics of magnetosomes confer them with signi...
Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that mineralize dissolved iron into intracellular magnetic crystals. After cell death, these crystals are trapped into sediments which removes iron from the soluble pool. MTB may significantly impact the iron biogeochemical cycle, especially in the ocean where dissolved iron limits...
Magnetotactic bacteria (MTB) are ubiquitous aquatic microorganisms that biomineralize dissolved iron from the environment into intracellular nanoparticles of magnetite [Fe(II)Fe(III) 2 O 4 ] or greigite [Fe(II)Fe(III) 2 S 4 ] in a genetically controlled manner. After cell death, these magnetite and greigite crystals are trapped into sediments which...
Magnetotactic bacteria (MTB) are a group of organisms that form intracellular nanometer-scale magnetic crystals though a complex process involving lipid and protein scaffolds. These magnetic crystals and their lipid membranes, termed magnetosomes, are model systems for studying bacterial cell biology and biomineralization and are potential platform...
Magnetosomes are complex bacterial organelles that serve as model systems for studying cell biology, biomineralization, and global iron cycling. Magnetosome biogenesis is primarily studied in two closely related Alphaproteobacterial Magnetospirillum spp. that form cubooctahedral-shaped magnetite crystals within a lipid membrane. However, chemically...
The formation of cellular magnetic dipoles by chain assemblies of stable single-domain magnetite nanocrystals is a characteristic feature in magnetotactic bacteria (MTB). The dipole strength depends on the competition or cooperation between the various anisotropic energy contributions, mainly between the magnetocrystalline and the interaction-induc...
Magnetotactic bacteria possess cellular compartments called magnetosomes that sense magnetic fields. Alignment of magnetosomes in the bacterial cell is necessary for their function, and this is achieved through anchoring of magnetosomes to filaments composed of the protein MamK. MamK is an actin homologue that polymerizes upon ATP binding. Here, we...
Magnetotactic bacteria are aquatic organisms that produce subcellular magnetic particles in order to orient in the earth's
geomagnetic field. MamE, a predicted HtrA protease required to produce magnetite crystals in the magnetotactic bacterium Magnetospirillum
magneticum AMB-1, was recently shown to promote the proteolytic processing of itself and...
Magnetotactic bacteria are aquatic organisms that produce subcellular magnetic particles in order to orient in the earth’s geomagnetic field. MamE, a predicted HtrA protease required to produce magnetite crystals in the magnetotactic bacterium Magnetospirillum magneticum AMB-1, was recently shown to promote the proteolytic processing of itself and...
Author
Biomineralization is an ancient and ubiquitous process by which organisms assemble crystalline materials for their own benefit. The ability to precisely organize inorganic atoms into crystals with intricate shapes demonstrates a level of control over nanoparticle synthesis that has fascinated biologists for generations. We have been studyin...
tmFRET data for Figs 6 and S7.
(XLSX)
Summary of crystallographic data.
(DOCX)
L1 loop conformation in a set of trypsin-like protease structures.
The main chain configuration at position 193 for all chains in the asymmetric unit of each structure was used to generate the table.
(DOCX)
Suggested renaming of the MamE clade.
The naming in a previous comparative genomic study is unconventional due to confusion over analogy to the MAI in α-Proteobacteria [12]. Our phylogenetic analysis clarifies the ancestry and allows us to use accepted nomenclature.
(DOCX)
Plasmids used in this study.
(DOCX)
Characterization of strains from Fig 3.
Stars indicate N-terminally 3xFLAG-tagged alleles throughout Fig 3. In the histograms, each measurement represents the average of three biological replicates. Error bars represent the standard deviation of the replicates. (A) Processing of MamO alleles used in this study in the ΔOΔR9 background. (B) Magnetic...
Cross-complementation of MamO protease domain mutants by LimO.
(A) limO is contained within a partially duplicated region of the mamAB cluster termed R9. While mamO is predicted to have a trypsin like-protease domain and a TauE-like transporter domain, limO has only a predicted trypsin-like domain with 98% identity to the N-terminus of mamO. LimO c...
Structure of the MamO protease domain.
(A) Schematic of the chymotrypsin fold with the loops and catalytic residues indicated. (B) Comparison of the L1 loop in MamO to the trypsin family consensus. (C) Overall structure of the MamO protease domain solved to 2.6 Å. The catalytic residues and bound peptides are show in stick representation.
(TIF)
Fluorescein-5-maleimide labeling of MamOQ258C.
(A) The fluorescent labeling site in MamO was chosen based on the optimum FRET distance from Taraska et al. [33] (B) Purification and fluorescent labeling of MamOQ258C and MamOQ258C H148A H263A.
(TIF)
tmFRET analysis of metal binding.
(A) Fluorescence quenching of MamO Q258C labeled with fluorescein-5-maleimide in the presence of increasing concentrations of NiSO4. (B) Binding of various transition metals to labeled MamO. Error bars represent the standard deviation from four independent measurements. The dotted lines are fits to the binding equa...
Biomineralization data for Figs 2, 6, S1, S2 and S3.
(XLSX)
Temperature dependence of magnetic response for mamO alleles in this study.
(TIF)
Similarity of the MamO metal binding site to equine kallikrein-3.
(A) F
O
-F
C omit map showing the bound Ni2+ ion in MamO. Blue: Ni2+; red: H2O; green: Cl-. (B,C) Comparison of metal binding sites in MamO and equine kallikrein-3. Coordinates of the zinc-bound structure reported in Carvahlo et al. [31] were not deposited in the PDB.
(TIF)
Alignment of the MamO family.
The conservation of critical residues discussed in the text is indicated with colored boxes.
(TIF)
Sample analysis of representative trypsin-like sequences from magnetotactic bacteria.
(A) Alignment of the catalytic loops from a set of trypsin-like sequences. The trypsin sequences from four magnetotactic organisms were aligned with two canonical HtrAs, H. sapiens HtrA1 and E. coli DegP. Positions of catalytic triad residues are marked with a sta...
Strains used in this study.
(DOCX)
Significance
Biomineralization is an important and widespread phenomenon by which living systems produce solid materials from soluble metal ions and has key implications with regard to environmental and health processes. In this work, we report studies of redox and structural components that control mineralization events in the production of iron n...
Magnetotactic bacteria (MTB) build magnetic nanoparticles in chain configuration to generate a permanent dipole in their cells as a tool to sense the Earth's magnetic field for navigation toward favorable habitats. The majority of known MTB align their nanoparticles along the magnetic easy axes so that the directions of the uniaxial symmetry and of...
Model genetic systems are invaluable, but limit us to understanding only a few organisms in detail, missing the variations in biological processes that are performed by related organisms. One such diverse process is the formation of magnetosome organelles by magnetotactic bacteria. Studies of model magnetotactic α-proteobacteria have demonstrated t...
Many bacterial species contain multiple actin-like proteins tasked with the execution of crucial cell biological functions.
MamK, an actin-like protein found in magnetotactic bacteria, is important in organizing magnetosome organelles into chains
that are used for navigation along geomagnetic fields. MamK and numerous other magnetosome formation fa...
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...
For many years bacteria were considered rather simple organisms, but the dogmatic notion that subcellular organization is a eukaryotic trait has been overthrown for more than a decade. The discovery of homologs of the eukaryotic cytoskeletal proteins actin, tubulin, and intermediate filaments in bacteria has been instrumental in changing this view....
of a paper presented at Microscopy and Microanalysis 2013 in Indianapolis, Indiana, USA, August 4 – August 8, 2013.
Magnetic imaging is a powerful tool for probing biological and physical systems. However, existing techniques either have poor spatial resolution compared to optical microscopy and are hence not generally applicable to imaging of sub-cellular structure (for example, magnetic resonance imaging), or entail operating conditions that preclude applicati...
We present recent work on developing a wide-field magnetic imaging system using the nitrogen-vacancy (NV) color center in diamond. The NV centers can function as a robust and bio-compatible magnetic sensor at room temperature. Optical detection of the spin state of NV centers allows magnetic field imaging with sub-micron spatial resolution. We use...
It is now recognized that actin-like proteins are widespread in bacteria and, in contrast to eukaryotic actins, are highly diverse in sequence and function. The bacterial actin, MamK, represents a clade, primarily found in magnetotactic bacteria, that is involved in the proper organization of subcellular organelles, termed magnetosomes. We have pre...
Magnetotactic bacteria (MTB) use magnetosomes, membrane-bound crystals of magnetite or greigite, for navigation along geomagnetic fields. In Magnetospirillum magneticum sp. AMB-1, and other MTB, a magnetosome gene island (MAI) is essential for every step of magnetosome formation. An 8-gene region of the MAI encodes several factors implicated in con...
Bacterial cells, like their eukaryotic counterparts, are capable of constructing lipid-based organelles that carry out essential biochemical functions. The magnetosomes of magnetotactic bacteria are one such compartment that is quickly becoming a model for exploring the process of organelle biogenesis in bacteria. Magnetosomes consist of a lipid-bi...
Developmental events across the prokaryotic life cycle are highly regulated at the transcriptional and posttranslational levels.
Key elements of a few regulatory networks are conserved among phylogenetic groups of bacteria, although the features controlled
by these conserved systems are as diverse as the organisms encoding them. In this work, we pr...
Magnetotactic bacteria (MB) are remarkable organisms with the ability to exploit the earth's magnetic field for navigational purposes. To do this, they build specialized compartments called magnetosomes that consist of a lipid membrane and a crystalline magnetic mineral. These organisms have the potential to serve as models for the study of compart...
Bacterial actins, in contrast to their eukaryotic counterparts, are highly divergent proteins whose wide-ranging functions are thought to correlate with their evolutionary diversity. One clade, represented by the MamK protein of magnetotactic bacteria, is required for the subcellular organization of magnetosomes, membrane-bound organelles that aid...
The magnetosome, a biomineralizing organelle within magnetotactic bacteria, allows their navigation along geomagnetic fields. Magnetosomes are membrane-bound compartments containing magnetic nanoparticles and organized into a chain within the cell, the assembly and biomineralization of magnetosomes are controlled by magnetosome-associated proteins....
Magnetotactic bacteria contain nanometre-sized, membrane-bound organelles, called magnetosomes, which are tasked with the biomineralization of small crystals of the iron oxide magnetite allowing the organism to use geomagnetic field lines for navigation. A key player in this process is the HtrA/DegP family protease MamE. In its absence, Magnetospir...
We developed a series of ligand-inducible riboswitches that control gene expression in diverse species of Gram-negative and
Gram-positive bacteria, including human pathogens that have few or no previously reported inducible expression systems. We
anticipate that these riboswitches will be useful tools for genetic studies in a wide range of bacteria...
Mounting evidence in recent years has challenged the dogma that prokaryotes are simple and undefined cells devoid of an organized subcellular architecture. In fact, proteins once thought to be the purely eukaryotic inventions, including relatives of actin and tubulin control prokaryotic cell shape, DNA segregation, and cytokinesis. Similarly, compa...
Intracellular magnetite crystal formation by magnetotactic bacteria has emerged as a powerful model for investigating the cellular and molecular mechanisms of biomineralization, a process common to all branches of life. Although magnetotactic bacteria are phylogenetically diverse and their crystals morphologically diverse, studies to date have focu...
Although membrane-bounded compartments are commonly considered a unique eukaryotic characteristic, many species of bacteria have organelles. Compartmentalization is well studied in eukaryotes; however, the molecular factors and processes leading to organelle formation in bacteria are poorly understood. We use the magnetosome compartments of magneto...
Magnetotactic bacteria are a diverse group of microorganisms with the ability to use geomagnetic fields for direction sensing. This unique feat is accomplished with the help of magnetosomes, nanometer-sized magnetic crystals surrounded by a lipid bilayer membrane and organized into chains via a dedicated cytoskeleton within the cell. Because of the...
Magnetosome chains are the intracellular structures that allow magnetotactic bacteria to align in
and navigate along geomagnetic fields (Bazylinski and Frankel 2004). These organelles are typically defined
as a unit consisting of a magnetite or greigite crystal surrounded by a lipid bilayer membrane
(Balkwill et al. 1980). Although these magnetic m...
Magnetosomes are membranous bacterial organelles sharing many features of eukaryotic organelles. Using electron cryotomography, we found that magnetosomes are invaginations of the cell membrane flanked by a network of cytoskeletal filaments. The filaments appeared to be composed of MamK, a homolog of the bacterial actin-like protein MreB, which for...
Magnetic bacteria synthesize nanoscale crystals of magnetite in intracellular, membrane-bounded organelles (magnetosomes). These crystals are preserved in the fossil record at least as far back as the late Neoproterozoic and have been tentatively identified in much older rocks (1). This fossil record may provide deep time calibration points for mol...
Magnetite is both a common inorganic rock-forming mineral and a biogenic product formed by a diversity of organisms. Magnetotactic bacteria produce intracellular magnetites of high purity and crystallinity (magnetosomes) arranged in linear chains of crystals. Magnetosomes and their fossils (magnetofossils) have been identified using transmission el...
Transmission electron microscopy studies have been used to argue that magnetite crystals in carbonate from Martian meteorite ALH84001 have a composition and morphology indistinguishable from that of magnetotactic bacteria. It has even been claimed from scanning electron microscopy imaging that some ALH84001 magnetite crystals are aligned in chains....