Dennis A. Bazylinski

Magnetosome formation in prokaryotes

Magnetotactic bacteria were discovered almost 30 years ago, and for many years and many different reasons, the number of researchers working in this field was few and progress was slow. Recently, however, thanks to the isolation of new strains and the development of new techniques for manipulating these strains, researchers from several laboratories have made significant progress in elucidating the molecular, biochemical, chemical and genetic bases of magnetosome formation and understanding how these unique intracellular organelles function. We focus here on this progress.

Rock magnetic criteria for the detection of biogenic magnetite

Abstract We report results on the magnetic properties of magnetites produced by magnetotactic and dissimilatory iron-reducing bacteria. Magnetotactic bacterial (MTB) strains MS1, MV1 and MV2 and dissimilatory iron-reducing bacterium strain GS-15, grown in pure cultures, were used in this study. Our results suggest that a combination of room temperature coercivity analysis and low temperature remanence measurements provides a characteristic magnetic signature for intact chains of single domain (SD) particles of magnetite from MTBs. The most useful magnetic property measurements include: (1) acquisition and demagnetization of isothermal remanent magnetization (IRM) using static, pulse and alternating fields; (2) acquisition of anhysteretic remanent magnetization (ARM); and (3) thermal dependence of low temperature (20 K) saturation IRM after cooling in zero field (ZFC) or in a 2.5 T field (FC) from 300 K. However, potentially the most diagnostic magnetic parameter for magnetosome chain identification in bulk sediment samples is related to the difference between low temperature zero-field and field cooled SIRMs on warming through the Verwey transition (T ≈ 100 K). Intact chains of unoxidized magnetite magnetosomes have ratios of δFC/δZFC greater than 2, where the parameter δ is a measure of the amount of remanence lost by warming through the Verwey transition. Disruption of the chain structure or conversion of the magnetosomes to maghemite reduces the δFC/δZFC ratio to around 1, similar to values observed for some inorganic magnetite, maghemite, greigite and GS-15 particles. Numerical simulations of δFC/δZFC ratios for simple binary mixtures of magnetosome chains and inorganic magnetic fractions suggest that the δFC/δZFC parameter can be a sensitive indicator of biogenic magnetite in the form of intact chains of magnetite magnetosomes and can be a useful magnetic technique for identifying them in whole-sediment samples. The strength of our approach lies in the comparative ease and rapidity with which magnetic measurements can be made, compared to techniques such as electron microscopy.

Elongated prismatic magnetite crystals in ALH84001 carbonate globules: Potential Martian magnetofossils

Using transmission electron microscopy (TEM), we have analyzed magnetite (Fe3O4) crystals acid-extracted from carbonate globules in Martian meteorite ALH84001. We studied 594 magnetites from ALH84001 and grouped them into three populations on the basis of morphology: 389 were irregularly shaped, 164 were elongated prisms, and 41 were whisker-like. As a possible terrestrial analog for the ALH84001 elongated prisms, we compared these magnetites with those produced by the terrestrial magnetotactic bacteria strain MV-1. By TEM again, we examined 206 magnetites recovered from strain MV-1 cells. Natural (Darwinian) selection in terrestrial magnetotactic bacteria appears to have resulted in the formation of intracellular magnetite crystals having the physical and chemical properties that optimize their magnetic moment. In this study, we describe six properties of magnetite produced by biologically controlled mechanisms (e.g., magnetotactic bacteria), properties that, collectively, are not observed in any known population of inorganic magnetites. These criteria can be used to distinguish one of the modes of origin for magnetites from samples with complex or unknown histories. Of the ALH84001 magnetites that we have examined, the elongated prismatic magnetite particles (similar to 27% of the total) are indistinguishable from the MV-1 magnetites in five of these six characteristics observed for biogenically controlled mineralization of magnetite crystals.

Anaerobic Magnetite Production by a Marine, Magnetotactic Bacterium

Bacterial production of magnetite represents a significant contribution to the natural remanent magnetism of deep-sea and other sediments1–5. Because cells of the freshwater magnetotactic bacterium Aquaspirillum magnetotacticum require molecular oxygen for growth and magnetite synthesis6, production of magnetite by magnetotactic bacteria has been considered to occur only in surficial aerobic sediments7. Moreover, it has been suggested that deposits of single-domain magnetite crystals are palaeooxygen indicators presumably having been formed under predominantly microaerobic conditions5–8. In contrast, some nonmagnetotactic, dissimilatory iron-reducing bacteria, such as the recently described strain GS-15 by Lovley et al.7, synthesize extracellular magnetite from hydrous ferric oxide under anaerobic conditions. We now report the first isolation and axenic culture of a marine, magnetotactic bacterium, designated MV-1, that can synthesize intracellular, single-domain magnetite crystals under strictly anaerobic conditions. We conclude that magnetotactic bacteria do not necessarily require molecular oxygen for magnetite synthesis and suggest that they, as well as dissimilatory iron-reducing bacteria, can contribute to the natural remanent magnetism of even long-term anaerobic sediments.

Biologically Induced Mineralization by Bacteria

Bacteria are small, prokaryotic, microorganisms that are ubiquitous in surface and subsurface terrestrial and aquatic habitats. Prokaryotes comprise two Domains (Superkingdoms) in the biological taxonomic hierarchy, the Bacteria and the Archaea. They exhibit remarkable diversity both genetically and metabolically even within the same microenvironment and they are thought to play a major role in the deposition and weathering of minerals in the earth’s crust. The synthesis of minerals by prokaryotes can be grouped into two canonical modes: 1) biologically induced mineralization (BIM) and 2) biologically controlled mineralization (BCM) (Lowenstam 1981; Lowenstam and Weiner 1989). In this chapter, we focus on biologically induced mineralization. Minerals that form by biologically induced mineralization processes generally nucleate and grow extracellularly as a result of metabolic activity of the organism and subsequent chemical reactions involving metabolic byproducts. In many cases , the organisms secrete one or more metabolic products that react with ions or compounds in the environment resulting in the subsequent deposition of mineral particles. Thus, BIM is a presumably unintended and uncontrolled consequence of metabolic activities. The minerals that form are often characterized by poor crystallinity , broad particle-size distributions, and lack of specific crystal morphologies. In addition , the lack of control over mineral formation often results in poor mineral specificity and/or the inclusion of impurities in the mineral lattice. BIM is, in essence, equivalent to inorganic mineralization under the same environmental conditions and the minerals are therefore likely to have crystallochemical features that are generally indistinguishable from minerals produced by inorganic chemical reactions. In some cases, the metabolic products diffuse away and minerals form from solution. However , bacterial surfaces such as cell walls or polymeric materials (exopolymers) exuded by bacteria, including slimes, sheaths, or biofilms, and even dormant spores, can act as important sites for the adsorption of ions …

Spatiotemporal Distribution of Marine Magnetotactic Bacteria in a Seasonally Stratified Coastal Salt Pond

ABSTRACT The occurrence and distribution of magnetotactic bacteria (MB) were studied as a function of the physical and chemical conditions in meromictic Salt Pond, Falmouth, Mass., throughout summer 2002. Three dominant MB morphotypes were observed to occur within the chemocline. Small microaerophilic magnetite-producing cocci were present at the top of the chemocline, while a greigite-producing packet-forming bacterium occurred at the base of the chemocline. The distributions of these groups displayed sharp changes in abundance over small length scales within the water column as well as strong seasonal fluctuations in population abundance. We identified a novel, greigite-producing rod in the sulfidic hypolimnion that was present in relatively constant abundance over the course of the season. This rod is the first MB that appears to belong to the γ-Proteobacteria, which may suggest an iron- rather than sulfur-based respiratory metabolism. Its distribution and phylogenetic identity suggest that an alternative model for the ecological and physiological role of magnetotaxis is needed for greigite-producing MB.

Comparative Genome Analysis of Four Magnetotactic Bacteria Reveals a Complex Set of Group-Specific Genes Implicated in Magnetosome Biomineralization and Function

Magnetotactic bacteria (MTB) are a heterogeneous group of aquatic prokaryotes with a unique intracellular organelle, the magnetosome, which orients the cell along magnetic field lines. Magnetotaxis is a complex phenotype, which depends on the coordinate synthesis of magnetosomes and the ability to swim and orient along the direction caused by the interaction with the Earths magnetic field. Although a number of putative magnetotaxis genes were recently identified within a conserved genomic magnetosome island (MAI) of several MTB, their functions have remained mostly unknown, and it was speculated that additional genes located outside the MAI might be involved in magnetosome formation and magnetotaxis. In order to identify genes specifically associated with the magnetotactic phenotype, we conducted comparisons between four sequenced magnetotactic Alphaproteobacteria including the nearly complete genome of Magnetospirillum gryphiswaldense strain MSR-1, the complete genome of Magnetospirillum magneticum strain AMB-1, the complete genome of the magnetic coccus MC-1, and the comparative-ready preliminary genome assembly of Magnetospirillum magnetotacticum strain MS-1 against an in-house database comprising 426 complete bacterial and archaeal genome sequences. A magnetobacterial core genome of about 891 genes was found shared by all four MTB. In addition to a set of approximately 152 genus-specific genes shared by the three Magnetospirillum strains, we identified 28 genes as group specific, i.e., which occur in all four analyzed MTB but exhibit no (MTB-specific genes) or only remote (MTB-related genes) similarity to any genes from nonmagnetotactic organisms and which besides various novel genes include nearly all mam and mms genes previously shown to control magnetosome formation. The MTB-specific and MTB-related genes to a large extent display synteny, partially encode previously unrecognized magnetosome membrane proteins, and are either located within (18 genes) or outside (10 genes) the MAI of M. gryphiswaldense. These genes, which represent less than 1% of the 4,268 open reading frames of the MSR-1 genome, as yet are mostly of unknown functions but are likely to be specifically involved in magnetotaxis and, thus, represent prime targets for future experimental analysis.

Truncated hexa-octahedral magnetite crystals in ALH84001: Presumptive biosignatures

McKay et al. [(1996) Science 273, 924–930] suggested that carbonate globules in the meteorite ALH84001 contained the fossil remains of Martian microbes. We have characterized a subpopulation of magnetite (Fe3O4) crystals present in abundance within the Fe-rich rims of these carbonate globules. We find these Martian magnetites to be both chemically and physically identical to terrestrial, biogenically precipitated, intracellular magnetites produced by magnetotactic bacteria strain MV-1. Specifically, both magnetite populations are single-domain and chemically pure, and exhibit a unique crystal habit we describe as truncated hexa-octahedral. There are no known reports of inorganic processes to explain the observation of truncated hexa-octahedral magnetites in a terrestrial sample. In bacteria strain MV-1 their presence is therefore likely a product of Natural Selection. Unless there is an unknown and unexplained inorganic process on Mars that is conspicuously absent on the Earth and forms truncated hexa-octahedral magnetites, we suggest that these magnetite crystals in the Martian meteorite ALH84001 were likely produced by a biogenic process. As such, these crystals are interpreted as Martian magnetofossils and constitute evidence of the oldest life yet found.

Ecology, Diversity, and Evolution of Magnetotactic Bacteria

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.

Magnetic Force Microscopy of the Submicron Magnetic Assembly in a Magnetotactic Bacterium

A magnetic force microscope (MFM) was used to image topography and magnetic forces from a chain of submicron single magnetic domain particles produced by and contained in isolated magnetotactic bacteria. The noncontact magnetic force microscope data were used to determine a value for the magnetic moment of an individual bacterial cell, of order 10−13 emu, consistent with the average magnetic moment of bacteria from the same sample, obtained by superconducting quantum interference device magnetometry. The results represent the most sensitive quantification of a magnetic force microscope image to date.