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Magnetotactic Bacteria (MTB) Adaptations

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Magnetotactic bacteria (MTB) are a polyphyletic group of motile bacteria that has been observed in freshwater and marine aquatic environments. Discovered in 1975 by Richard Blakemore, these microorganisms are able to passively navigate along the earth’s magnetic field toward the bottom of their aquatic habitats, to efficiently find low oxygen environments. The MTB passive navigation is enabled by the biomineralization of crystals of the iron oxide magnetite (Fe3O4) or, in some cases, the iron sulfide greigite (Fe3S4). These crystals are enveloped in a specialized, bilayer membrane organelle named the magnetosome (Komeili, 2012).

MTB are not pulled northward or southward by the magnetic field, they are only aligned and swim parallel to it. North seeking MTB are found in the northern hemisphere; whereas, south-seeking MTB are found in the southern hemisphere (Blakemore, 1982).

Surveys describing the ecology of MTB show that they are found in the highest numbers close to the oxic anoxic transition zone (OATZ), an habitat where opposing horizontal gradients of reduced compounds (usually sulfide from the bottom of sediments) and oxidized compounds (oxygen, diffusing from the surface of the aquatic environment) are present. (Komeili, 2012).

When coupling these observations, it is clear to see how the magnetosome organelle is advantageous to the MTB - By using the earth’s magnetic field as a vertical guide through the horizontal opposing gradients, these bacteria use a one-dimensional, simpler route to finding the OATZ, rather than the labyrinthine, three dimensional chemotactic or aerotactic search mechanisms (Komeili, 2012).

Synthesized through an invagination process from the cell's inner membrane, the magnetosomes are intracellular, bilayer membrane organelle that provides both spatial and physicochemical control over the magnetic crystals biomineralization (Komeili, 2012). Through strict genetic control mechanisms, the magnetosomes are organized into highly ordered intracellular chains (one to several), which is essential for the ability of the cell to align with the earth's magnetic field. The biomineralization process in magnetosomes is also genetically controlled, leading to a similarity of crystal's size, shape and number within a single bacterial strain (Komeili, 2012).

Since Blakemore’s serendipitous discovery of the MTB, these unique bacteria are of considerable research interest and the magnetosome formation and biomineralization has evolved into an interdisciplinary field of research. In recent years, great effort to find the molecular basis of the magnetosome synthesis and biomineralization has resulted in a fuller understanding of this process. To answer the question just how well adapted are these organisms to align with the earth's magnetic field, I will present the possible molecular mechanisms of cytoskeletal organization and biomineralization that allows for the formation of a functional magnetosome organelle.

The efficiency of the MTB magnetic response largely depends on the total magnetic dipole moment that the cell exhibits. To maximize the magnetic moment dipole, first, they must precisely control the biomineralization of a magnetite crystal within the single magnetic domain size range, meaning that the crystals enveloped by the magnetosome should be characterized by a stable and uniform magnetization, in a way that the magnetic moment of the particle attains a maximum value. Therefore, these crystals exhibit narrow size distributions where mature crystals typically fall within the range of about 35–120 nm (Komeili, 2012). Smaller superparamagnetic particles would not efficiently contribute to the cellular magnetic moment at ambient temperature, whereas larger crystals tend to reduce their total magnetic moment because they naturally form multiple magnetic domains (Komeili, 2012).

Second, to truly function as a compass needle, the magnetosomes needs to be arranged in a linear fashion into chains to achieve the maximum possible magnetic moment. Without this chain structure, magnetosomes have the tendency to agglomerate in order to reduce the system's energy (Scheffel, 2006). The magnetosome chains are built on a filament cytoskeletal structures that run along the length of the MTB and orient the magnetic dipole moments of the particles parallel to each other along the chain. The total magnetic dipole moment is then the sum of the moments of the individual particles, thus constructing a permanent magnetic dipole large enough to align the MTB with earth's magnetic field (Scheffel, 2006).

Recent genetic studies of MTB have led to the identification of a large area named the magnetosome gene island (MAI). This island contains many of the genes that encode most of the magnetosome membrane proteins, which in turn, are responsible for forming a functioning organelle (Scheffel, 2006). Genetic studies of two MAI genes, mamJ and mamK, have revealed that they play a key role in the formation and stability of the magnetosome chain (Komeili, 2012).

mamK, is predicted to code a bacterial actin-like protein that form the cytoskeletal chains filament. To test this assumption, a mutant MTB was generated using an inframe deletion mutation of the mamK gene (Komeili, 2005).

The deletion of the mamK gene did not affect the biomineralization or the magnetosomes formation and the mutant continued to form magnetite crystals. However, the magnetosomes were dispersed in the cell cytoplasm and did not organize as one coherent chain (Komeili, 2005). To ensure that this phenotype is due to the deletion of mamK, a plasmid carrying the mamK gene was introduced to the mutants, and some of the cells showed full reversal of the mutant phenotype (Komeili, 2005). These results could indicate that MamK codes for the long filament that organizes and maintains the magnetosomes in a coherent chain structure.

mamK and mamJ genes are located consecutively on the MTB genome and are co-transcribed (Scheffel, 2006). To test the role of the mamJ gene in the biomineralization process of MTB, a mutant was generated in which the mamJ gene was removed through an inframe deletion mutation. Magnetite biomineralization was not affected and the mutant continued to form magnetite crystals (Scheffel, 2006). The magnetosome associated cytoskeletal filament that forms the chain was still present in the mamJ mutant strain, but the magnetosomes were not attached to the chain and were dispersed in the cell's cytoplasm (Scheffel, 2006). Thus, when combining the results from both experiments described above, it appears that that mamJ, while not responsible for the formation of the cytoskeletal filaments, works in cooperation with mamK and mediates the interaction between the magnetosome and the cytoskeletal filaments (Komeili, 2012).

These results demonstrate that in order to achieve a high structural level that allows for functional magnetotactic ability, the magnetosome chain assembly is strictly genetically controlled. In terms of cellular organization, the MTB magnetotactic ability is among the most elaborated prokaryotic traits (Komeili, 2012). Understanding this cellular organization and its genetic control mechanisms in a model organism such as the MTB, could lead to innovative treatments for diseases in which magnetite is linked to a pathological conditions. For example, defects in the protein ferritin causes patients who suffer from the genetic neurodegenerative disorder, neuroferritinopathy, to accumulate magnetite in the brain (Komeili, 2012). A clearer understanding of the genetic control that governs the MTB magnetotactic ability could lead to insights into the molecular biology of this disorder.

References

Blakemore, R. P. 1982. Magnetotactic bacteria. Annu. Rev. Microbiol. 36:217-238.

Komeili, A., Z. Li, D. K. Newman, and G. J. Jensen.2005. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK.Science311:242-245

Komeili, A. “Molecular Mechanisms of Compartmentalization and Biomineralization in Magnetotactic Bacteria.”FEMS microbiology reviews36.1 (2012): 232–255.PMC. Web. 23 June 2015.

Scheffel, M. Gruska, D. Faivre, A. Linaroudis, J.M. Plitzko, D. Schuler An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria Nature, 440 (2006), pp. 110–114


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