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Magnetosome biogenesis in magnetotactic bacteria

Key Points

  • The orientation of magnetotactic bacteria is based on the presence of unique organelles, magnetosomes, which are intracellular, membrane-enclosed, nanometre-sized crystals of magnetic iron minerals.

  • In the past decade, substantial advances have been made in our understanding of magnetosome biogenesis using two genetically tractable Magnetospirillum species.

  • Magnetosome biogenesis entails the invagination of the magnetosome membrane, recruitment of specific proteins, iron transport and redox-controlled biomineralization of magnetite crystals; magnetosomes are then assembled and positioned into well-ordered linear chains that are among the most complex structures seen in prokaryotic organisms.

  • Key functions of magnetosome biogenesis are encoded by about 30 genes that are clustered in a genomic 'magnetosome island', although additional auxiliary functions are contributed by general cellular metabolic and regulatory pathways, including aerobic and anaerobic respiration.

  • A non-magnetotactic bacterium has recently been 'magnetized' through the heterologous expression of genes that encode the magnetosome biogenesis pathway, which is a proof-of-principle demonstration that non-magnetotactic bacteria that are more facile for laboratory investigation could be 'magnetized' to provide new models for genetic dissection and synthetic biology.

  • Bacterial magnetosomes are promising nanomaterials for various bioremediation, biomedical and bionanotechnological applications.

Abstract

Magnetotactic bacteria derive their magnetic orientation from magnetosomes, which are unique organelles that contain nanometre-sized crystals of magnetic iron minerals. Although these organelles have evident potential for exciting biotechnological applications, a lack of genetically tractable magnetotactic bacteria had hampered the development of such tools; however, in the past decade, genetic studies using two model Magnetospirillum species have revealed much about the mechanisms of magnetosome biogenesis. In this Review, we highlight these new insights and place the molecular mechanisms of magnetosome biogenesis in the context of the complex cell biology of Magnetospirillum spp. Furthermore, we discuss the diverse properties of magnetosome biogenesis in other species of magnetotactic bacteria and consider the value of genetically 'magnetizing' non-magnetotactic bacteria. Finally, we discuss future prospects for this highly interdisciplinary and rapidly advancing field.

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Figure 1: Overview of the mechanisms and genetics of magnetosome biogenesis.
Figure 2: Magnetosome membrane invagination and protein recruitment.
Figure 3: Biomineralization of magnetite crystals.
Figure 4: Magnetosome chain assembly, positioning and segregation.
Figure 5: Diversity and genetic engineering of magnetosomes.

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Acknowledgements

The authors thank their co-workers and colleagues for helpful discussions. Work in the Schüler laboratory is supported by grants from the Human Frontier Science Program (HFSP), the Deutsche Forschungsgemeinschaft and the European Research Council (ERC).

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Glossary

Microoxic

A concentration of oxygen that is less than 21% and therefore lower than that found in the atmosphere.

Biomineralization

The process by which organisms form inorganic minerals.

Aerotaxis

Movement of an organism towards (positive) or away (negative) from oxygen.

Chemoreceptors

Proteins that detect certain chemical stimuli in the environment.

Genomic islands

Discrete genomic regions that can be transferred horizontally. These genomic regions typically encode several transposases and integrases to increase the rate of DNA turnover and are frequently associated with the adaptation of microorganisms to new environments.

Cation diffusion facilitator

(CDF). A ubiquitous family of proteins that transport divalent metal cations (such as Zn2+, Mn2+, Cd2+, Co2+ and Fe2+) using a proton or potassium antiport mechanism.

Tetratricopeptide repeat

(TPR). A structural motif of 34 degenerate amino acids that is often involved in the assembly of multiprotein complexes by mediating protein–protein interactions.

Landmark protein

Proteins that mark certain cellular regions (or structures) and that may direct the assembly of larger multiprotein complexes.

PDZ domain

A short (80–90 amino acids) protein domain that is often involved in organizing signalling complexes by forming protein–protein interactions with carboxy-terminal peptides. The name derives from the proteins in which the domain was first described: postsynaptic density protein 95 (PSD95), discs large homologue 1(Dlg1) and zonula occludens 1 (ZO-1).

Mössbauer spectroscopy

A spectroscopic technique that is based on the Mössbauer effect, which is the nearly recoil-free, resonant absorption and emission of gamma rays in solids.

Major facilitator superfamily

(MFS). A family of ubiquitous membrane proteins that transports sugars, oligosaccharides, amino acids, peptides, drugs, metal ions and oxyanions, either across an electrochemical (uniporter) or a chemiosmotic (symporter or antiporter) gradient.

Magnetic heating

The process of heat release by magnetic nanoparticles that are exposed to alternating magnetic fields.

Colloidal stability

The tendency of particles to remain suspended in solution.

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Uebe, R., Schüler, D. Magnetosome biogenesis in magnetotactic bacteria. Nat Rev Microbiol 14, 621–637 (2016). https://doi.org/10.1038/nrmicro.2016.99

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