Magnetotactic Bacteria

Figure 1- Electron micrograph of Magnetospirillum gryphiswaldense cells containing chains of magnetite crystals (top) and magnified section of crystal chain (bottom). By Caulobacter subvibrioides (Diskussion) GFDL (http://www.gnu.org/copyleft/fdl.html)], via Wikimedia Commons

Magnetotactic bacteria (MB) are gram-negative bacteria that build specialized organelles called magnetosomes to store magnetic material. These magnetosomes are composed of a lipid membrane and crystalline magnetic mineral in the form of magnetite (Fe₃O₄) or greigite (Fe₃S₄). Magnetotactic bacteria are a very interesting research topic because they have the potential to impact a large number of scientific and applied disciplines. Magnetosomes are the perfect model for the study of cellular compartmentalization and organization in bacteria because the formation of specialized, membrane bound, features is usually attributed to eukaryotic organisms. Magnetotactic bacteria are also a great model for the study of biomineralization because of the precise control over the composition, size and morphology of magenetite crystals in magnetosomes.

Introduction

Figure 2 - Model of magneto-aeotaxis. Magnetotactic bacteria (black) use the earth's magnetic field (gray lines) as guides to localize to the OATZ while other organisms (white) must rely on other methods for finding the same region. Courtesy of Komeili (http://femsre.oxfordjournals.org/content/36/1/232.figures-only)

Magnetotactic bacteria were first described in 1975 when Richard Blakemore realized that a specific group of bacteria collected from sediment constantly swam in the same geographic direction, regardless of the positioning of the microscope or external stimuli.^[1] MB are mostly found in shallow aquatic environments where oxygen and other redox compounds are horizontally stratified. Many described magnetotactic bacteria localize at or close to the oxic anoxic transition zone (OATZ)—a region in the water column that has very low oxygen levels. ^[2] The current model (shown in Figure 2) to explain the selective advantage provided by magnetosomes is that magnetotactic bacteria are able to locate the OATZ much easier than bacteria that solely use chemotactic and aerotactic mechanisms. ^[3] Although the magneto-aerotaxis model has been widely accepted amongst the scientific community, new research is suggesting that the behavior magnetotactic bacteria exhibit in the environment may be more complicated than a simple response to oxygen levels:

Some MB species also show phototactic response, which helps reinforce magneto-aerotactic behavior and repel them from surface waters ^{[4, 5]}
Genome sequences show that MB have some of the highest numbers of signaling proteins of Bacteria ^[6]
MB produce more magnetosomes than necessary to align with the earth’s magnetic field ^[7]
MB have been found near the equator, where their magneto-aerotactic behavior has no advantage ^[8]

The Magnetosome Island

Bacterial genomes can evolve over time due to mutations, rearrangements, or horizontal gene transfer and many genes that are acquired through horizontal gene transfer come in blocks that are recognized as genomic islands. These genomic islands can be recognized by nucleotide statistics (GC skew) that differ from the rest of the organisms DNA and are often associated with inserted tRNA genes, pseudogenes, transposons, and IS elements.^[9] The gene clusters encoding the majority of magnetosome proteins have many hallmarks of genomic islands and, as a result, have been termed the magnetosome gene island (MAI).^[10] In one species of magnetotactic bacteria, Magnetospirillum magneticum (AMB-1), the MAI is approximately 98 kb long, encodes approximately 100 proteins, and represents over 2% of the bacterium's genetic material.^[11] Although the MAI does not have any clear boundaries, it is estimated to be even larger in other cultured strains of magnetotactic bacteria and research suggests that specific mechanisms may be in place to delete the MAI under stressful conditions due to the large energetic burden it creates for the organism.^[10]

MAI genes are required in multiple steps of magnetosome formation. Phylogenetic comparisons of magnetotactic bacteria use the highly conserved mam genes to trace the evolutionary history of magnetosome formation. MAI genes have been found in some of the most evolutionarily diverse species of magnetotactic bacteria, and there are multiple interpretations of what this could mean in terms of the evolution of magnetosome formation:^[11]

magnetosome formation was invented only once during evolution
magnetosome genes spread to diverse bacterial clades through ancient horizontal gene transfer
the last common ancestor of the Proteobacteria and the Nitrospira may have been magnetotactic bacteria and many species of the two groups lost their magnetosome genes over time

Most magnetosome research has focused on the model strains of MB that can be cultured in laboratories, but there are many fascinating variations of magnetosome morphology and organization that are found outside these model species. Researchers are able to use high-throughput sequencing technologies to identify the MAI of uncultured MB. One uncultured strain, Magnetobacterium bavaricum (Mbav), is the most phylogenetically distant of the well characterized magnetotactic bacteria and forms hundreds of tooth shaped crystals arranged in multiple strands within the cell. ^[3] In one study, the DNA of Mbav cells was extracted, amplified, and sequenced and the researchers were able to identify a genomic segment with the characteristics of the mamAB gene cluster found in other magnetotactic bacteria.^[11]

Magnetosome Formation

Figure 3- Proposed model of magnetosome formation. "First, the reshaping of the inner cell membrane by MamI, MamL, MamQ, MamB, and other factors (green) creates the magnetosome membrane. Second, MamE is recruited to the nascent magnetosome. Third, MamE (in blue), independent of its protease activity recruits other proteins (red) to the magnetosome. Fourth, MamK and MamJ help to organize magnetosomes into chains. Note that this step is independent of biomineralization and may occur before or after crystal formation. Fifth, biomineralization is initiated, and small crystals of magnetite are formed. Finally, these small crystals are matured into large crystals in a step that requires the proteolytic activity of MamE." Komeili (2012) Courtesy of Komeili (http://femsre.oxfordjournals.org/content/36/1/232.figures-only)

Identification of the genetic elements needed for magnetosome formation took many years due the lack of cultured and genetically tractable model organisms. Aquaspirillum magnetotacticum, now referred to as Magnetospirillum magnetotacticum, or MS-1, was the first magnetotactic bacteria to be isolated in pure culture. Two closely related Magnetospirillum species, Magnetospirillum grysphiswaldense (MSR-1) and Magnetospirillum magneticum (AMB-1), were isolated soon after and have become the focus of most magnetosome formation research.^[12,13] Three approaches have been used to determine the molecular factors involved in the formation of magnetosomes: proteomics, genetic analysis, and comparative genomics.

Membrane Biogenesis and Protein Sorting

The magnetosome membrane is an independent structure that provides the proper chemical environment for biomineralization and protects the rest of the cell from any toxic byproducts of biomineralization. Multiple studies have shown magnetosome membrane formation even when iron is eliminated from the growth medium, suggesting that these structures form regardless of environmental conditions.^[3] Electron cryotomography (ECT) has been used to generate high resolution views of the structure and organization of magnetosomes within MB. Recently, Komeili and Arash used ECT to show that magnetosome membranes are invaginations of the inner cell membrane. ^[14]

Chain Formation

Biomineralization

Biomineralization is the process in which organisms produce minerals, usually for some biological function. Magnetotactic bacteria form magnetosomes in order to provide a compartment to safely and efficiently direct the formation of magnetite crystals. The first step in magnetite biomineralization is the transport of iron into the cell.

Research Applications

Bioremediation

Conventional methods of remediation such as chemical precipitation, ion exchange, and active carbon adsorption have been used to clean up contaminated sites, but these methods are commonly associated with high costs, low efficiency, and problems with secondary pollution. In recent years, a lot of bioremediation research has focused on biosorbents because of their low cost, high availability, and great adsorption properties. One of the greatest challenges with using Biosorbents in bioremediation is that they are notoriously difficult to recover in the field. Magnetotactic bacteria, however, are very promising because they can easily be separated from wastewater due to their magnetic properties.

Barriers

Bioremediation is a very knowledge-intensive process and strategies often differ from site to site. Aside from individual site analysis, there is still a lot of research that could be done to better understand to underlying processes involved in the biomineralization and biosorption in magnetotactic bacteria and increase efficiency of remediation: