Abstract
Most organisms are simply diamagnetic, while magnetotactic bacteria and migratory animals are among organisms that exploit magnetism. Biogenic magnetization not only is of fundamental interest, but also has industrial potential. However, the key factor(s) that enable biogenic magnetization in coordination with other cellular functions and metabolism remain unknown. To address the requirements for induction and the application of synthetic bio-magnetism, we explored the creation of magnetism in a simple model organism. Cell magnetization was first observed by attraction towards a magnet when normally diamagnetic yeast Saccharomyces cerevisiae were grown with ferric citrate. The magnetization was further enhanced by genetic modification of iron homeostasis and introduction of ferritin. The acquired magnetizable properties enabled the cells to be attracted to a magnet, and be trapped by a magnetic column. Superconducting quantum interference device (SQUID) magnetometry confirmed and quantitatively characterized the acquired paramagnetism. Electron microscopy and energy-dispersive X-ray spectroscopy showed electron-dense iron-containing aggregates within the magnetized cells. Magnetization-based screening of gene knockouts identified Tco89p, a component of TORC1 (Target of rapamycin complex 1), as important for magnetization; loss of TCO89 and treatment with rapamycin reduced magnetization in a TCO89-dependent manner. The TCO89 expression level positively correlated with magnetization, enabling inducible magnetization. Several carbon metabolism genes were also shown to affect magnetization. Redox mediators indicated that TCO89 alters the intracellular redox to an oxidized state in a dose-dependent manner. Taken together, we demonstrated that synthetic induction of magnetization is possible and that the key factors are local redox control through carbon metabolism and iron supply.
Highlights
In biology, magnetism is a unique and virtually orthogonal physical property
Specific genes are crucial for the formation of these magnetic particles, but no such genes have yet been characterized in migratory animals
We find that yeast cells expressing a set of human proteins that sequester iron contain iron particles and become attracted by a magnet when grown with ferric citrate
Summary
Magnetism is a unique and virtually orthogonal physical property. As magnetic interactions can be contactless, remote, and permeable, integration of magnetic properties into biological systems provides another dimension for bioengineering and therapy. Magnetotactic bacteria produce a chain of organelles called magnetosomes [1], in which ferromagnetic magnetite (Fe3O4) or greigite (Fe3S4) particles are formed (reviewed in [2]). A putative iron transporter gene MagA from magnetotactic bacteria [5] has been shown to be sufficient for producing MRI-detectable ironcontaining particles in mammalian cells [6,7]. Members of magnetotactic bacteria identified so far belong to aproteobacteria, d-proteobacteria, Nitrospira (reviewed in [2]), and c-proteobacteria [10], while intracellular magnetic inclusions were found in Shewanella putrefaciens [11] and a photosynthetic purple bacteria [12] and a geo-biological study has presented magneto-fossils that are too large for bacteria—a possible remnant of eukaryotic biogenic magnetic particles [13]
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