Synthesis of the bacterial magnetosome: the making of a magnetic personality

Magnetotactic bacteria synthesize intracellular, enveloped, single magnetic domain crystals of magnetite Fe3O4, Fe2+Fe23+O4) and/or greigite (Fe3S4) called magnetosomes. The magnetosomes contain well-ordered crystals that have narrow size distributions and consistent species- and/or strain-specific morphologies. These characteristics are features of a process called biologically-controlled mineralization in which an organism exerts a great degree of crystallochemical control over the nucleation and growth of the mineral particle. Because of these features, the mineral particles have been used as biomarkers although not without controversy. These unique structures impart a permanent magnetic dipole moment to the cell causing it to align and swim along geomagnetic field lines, a behavior known as magnetotaxis. The apparent biological advantage of magnetotaxis is that it aids cells in more efficiently locating and maintaining position in vertical chemical gradients common in many natural aquatic environments

Magnetotaxis and Magnetic Particles in Bacteria

Magnetotactic bacteria contain magnetic particles that constitute a permanent magnetic dipole and cause each cell to orient and migrate along geomagnetic field lines. Recent results relevant to the biomineralization process and to the function of magnetotaxis are discussed

Magnetosome genes in the Gammaproteobacterium strain BW-2

Magnetotactic bacteria (MTB) biomineralize intracellular nanometer-sized, magnetic crystals surrounded by a lipid bilayer membrane known as magnetosomes. These crystals, which consist of magnetite (Fe3O4) or greigite (Fe3S4), causes the cell to align along the geomagnetic field lines as they swim, a phenomenon known as magnetotaxis. Strain BW-2 is a magnetite-producing magnetotactic bacterium isolated from Badwater Basin, Death Valley National Park (California) and is one of only two species of MTB that are known to phylogenetically belong to the Gammaproteobacteria class of the Proteobacteria phylum. The biomineralization of magnetite in magnetotactic bacteria is mediated by a series of genes that include the mam, mms, and mtx genes that presumably control the production of and the size and shape of the magnetite crystal within the magnetosomes. Magnetosome genes have not yet been found in the genomes of newly discovered magnetotactic Gammaproteobacteria. In this study, we use polymerase chain reaction with degenerate primers designed from mam genes found in other MTB, and DNA sequencing to search for and amplify possible mam genes in the Gammaproteobacterium strain BW-2. In addition, with enough DNA sequence, we may be able to find evidence of the presence of a magnetosome gene island in this organism. Positive results from this study will be instrumental in determining evidence for lateral gene transfer of the magnetosome gene island to the Gammaproteobacteria and the evolution of magnetotaxis based on magnetite biomineralization in general

Phylogenetic studies of newly isolated freshwater Magnetospirilla using cbb and mam genes

The phylogeny and general relatedness of prokaryotes is determined by comparisons of the sequences of rRNA genes, most commonly the 16S rRNA gene. Comparisons between other gene sequences have been used for this purpose and some have supported conclusions from 16S rRNA genes while others have not. In this study, 13 new magnetospirilla were phylogenetically characterized using the sequences of the 16S rRNA gene as well as the genes for forms I and II ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO) (cbbL and cbbM, respectively) and for two magnetosome membrane proteins unique to magnetotactic bacteria, mamJ and mamK. Polymerase chain reaction (PCR) with degenerate primers designed for the specific genes under study was used to amplify a large portion of the genes. PCR products were cloned and sequenced and used for the construction of phylogenetic trees. Based on 16S rRNA gene sequences, the magnetospirilla phylogenetically span, more as a continuum rather than as clearly delineated groups, over two genera based on the current accepted sequence divergence between organisms for genera (\u3e5%). While almost all strains appear to fit into the genus Magnetospirillum, strain LM-1 appears to represent a new genus. Phylogeny of these strains based on cbbM sequences was reasonably consistent with that from 16S rRNA genes. The cbbL gene was not a good choice for this study as most strains did not possess this gene. Relatedness and phylogeny of the strains based on mamJ and mamK sequences was more complex. Although our data set is not complete, some specific strains shown to be closely related by 16S rRNA gene sequence, also appeared to be closely related based on one or both of the mam gene sequences (e.g., strains UT-1, LM-2 and M. gryphiswaldense strain MSR-1). Other strains did not show this type of relationship. Because of these somewhat inconsistent results, those from mam gene sequences might reflect evolution of the magnetosome gene island (MAI) in magnetospirilla rather than relatedness between strains

Biomineralization of Magnetic Iron Minerals in Bacteria

Magnetotactic bacteria orient and migrate along magnetic field lines. This ability is based on a submicron assembly of single-magnetic domain iron mineral particles that elegantly solves the problem of how to construct a magnetic dipole that is large enough to be oriented in the geomagnetic field at ambient temperature, yet fit inside a micron-sized cell. The solution is based on the ability of the bacteria to accumulate high concentrations of iron, and control the deposition, size and orientation of a specific iron mineral at specific locations in the cell

Magnetic irreversibility and Verwey transition in nano-crystalline bacterial magnetite

The magnetic properties of biologically-produced magnetite nanocrystals biomineralized by four different magnetotactic bacteria were compared to those of synthetic magnetite nanocrystals and large, high quality single crystals. The magnetic feature at the Verwey temperature, $T_{V}$, was clearly seen in all nanocrystals, although its sharpness depended on the shape of individual nanoparticles and whether or not the particles were arranged in magnetosome chains. The transition was broader in the individual superparamagnetic nanoparticles for which $T_{B}<T_{V}$, where $T_{B}$ is the superparamagnetic blocking temperature. For the nanocrystals organized in chains, the effective blocking temperature $T_{B}>T_{V}$ and the Verwey transition is sharply defined. No correlation between the particle size and $T_{V}$ was found. Furthermore, measurements of $M(H,T,time)$ suggest that magnetosome chains behave as long magnetic dipoles where the local magnetic field is directed along the chain and this result confirms that time-logarithmic magnetic relaxation is due to the collective (dipolar) nature of the barrier for magnetic moment reorientation

Aerobic respiration by two Sulfate reducing magnetotactic bacteria, strains RS-1 and FH-1

Magnetotactic bacteria is the categorical name for a group of prokaryotes that biomineralize magnetosomes which are intracellular, membrane-bounded magnetic iron mineral crystals. The focus of this study is on two magnetiteproducing, magnetotactic sulfate-reducing bacteria (SRB), Desulfovibrio magneticus strain RS-1 and strain FH-1 which also belongs in the genus Desulfovibrio in the δ-Proteobacteria. SRB utilize sulfate as a terminal electron acceptor under anaerobic conditions reducing sulfate to sulfide. A large number of organic compounds as well as some inorganic compounds have been shown to provide electrons for sulfate reduction. Traditionally, because no SRB have been shown to convincingly grow with O2 as a terminal electron acceptor, they have been classified as obligate anaerobes. In characterizing several magnetotactic SRB, we found that cells of D. magneticus and strain FH-1 utilized O2 as an electron acceptor for growth. To prove this we grew cells of both strains in several different semi-solid growth media under air or N2 gas. Cells of both strains grew as a microaerophilic band of cells at the oxic-anoxic interface (OAI) in media under air lacking sulfate (medium contained cysteine or cysteine with either Casamino Acids or Yeast Extract as a sulfur source). Sulfide (as FeS: high [Fe] was used as a trap for sulfide) was not produced in these tubes. Cells did not grow under anaerobic conditions (under N2) in this medium unless sulfate was present. When sulfate was present in the growth medium, under air, initial growth of the strains was also as a microaerophilic band of cells at the OAI. However as time went on, the band of D. magneticus split into two. The band of FH-1 cells did not split into two bands and moved up the tube almost to the meniscus. The medium also turned dark indicating sulfide production. The results show that these magnetotactic SRB strains are capable of aerobic growth with O2 as a terminal electron acceptor

Magnetosome Gene Duplication as an Important Driver in the Evolution of Magnetotaxis in the Alphaproteobacteria

The evolution of microbial magnetoreception (or magnetotaxis) is of great interest in the fields of microbiology, evolutionary biology, biophysics, geomicrobiology, and geochemistry. Current genomic data from magnetotactic bacteria (MTB), the only prokaryotes known to be capable of sensing the Earth’s geomagnetic field, suggests an ancient origin of magnetotaxis in the domain Bacteria. Vertical inheritance, followed by multiple independent magnetosome gene cluster loss, is considered to be one of the major forces that drove the evolution of magnetotaxis at or above the class or phylum level, although the evolutionary trajectories at lower taxonomic ranks (e.g., within the class level) remain largely unstudied. Here we report the isolation, cultivation, and sequencing of a novel magnetotactic spirillum belonging to the genus Terasakiella (Terasakiella sp. strain SH-1) within the class Alphaproteobacteria. The complete genome sequence of Terasakiella sp. strain SH-1 revealed an unexpected duplication event of magnetosome genes within the mamAB operon, a group of genes essential for magnetosome biomineralization and magnetotaxis. Intriguingly, further comparative genomic analysis suggests that the duplication of mamAB genes is a common feature in the genomes of alphaproteobacterial MTB. Taken together, with the additional finding that gene duplication appears to have also occurred in some magnetotactic members of the Deltaproteobacteria, our results indicate that gene duplication plays an important role in the evolution of magnetotaxis in the Alphaproteobacteria and perhaps the domain Bacteria

The Characterization of two diverse magnetotactic bacteria: LEMS and MMS-1

Magnetotactic bacteria (MTB) are a diverse group of prokaryotes that biomineralize membrane-bound magnetic crystals known as magnetosomes. The magnetosomes are aligned within the cell and consist of either magnetite (Fe3O4) or greigite (Fe3S4). The biomineralization of magnetosomes consists of several processes including: invagination of the cytoplasmic membrane, iron uptake into the cell and then into the magnetosome membrane vesicle, and crystallization of the mineral phase inside the vesicle. Mam genes control magnetosome biomineralization with most of the genes present in an island called a magnetosome island. Many of the mam genes are conserved between different species of MTB. The genes that are in the island have suggested that they play a significant role in the organization of the magnetosomes and how they align within the cell. The focus of this investigation is to determine if certain conserved mam genes are found in two isolated and metabolically diverse magnetotactic spirillums: LEMS and MMS-1