Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters

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Abstract

The synthetic production of monodisperse single magnetic domain nanoparticles at ambient temperature is challenging1,2. In nature, magnetosomes—membrane-bound magnetic nanocrystals with unprecedented magnetic properties—can be biomineralized by magnetotactic bacteria3. However, these microbes are difficult to handle. Expression of the underlying biosynthetic pathway from these fastidious microorganisms within other organisms could therefore greatly expand their nanotechnological and biomedical applications4,5. So far, this has been hindered by the structural and genetic complexity of the magnetosome organelle and insufficient knowledge of the biosynthetic functions involved. Here, we show that the ability to biomineralize highly ordered magnetic nanostructures can be transferred to a foreign recipient. Expression of a minimal set of genes from the magnetotactic bacterium Magnetospirillum gryphiswaldense resulted in magnetosome biosynthesis within the photosynthetic model organism Rhodospirillum rubrum. Our findings will enable the sustainable production of tailored magnetic nanostructures in biotechnologically relevant hosts and represent a step towards the endogenous magnetization of various organisms by synthetic biology.

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Figure 1: Schematic representation of molecular organization of gene cassettes inserted into the chromosome of R. rubrum in a stepwise manner.
Figure 2: Phenotypes of R. rubrum strains expressing different magnetosome gene clusters and auxiliary genes.
Figure 3: Ultrastructural analysis of R. rubrum_ABG6X and isolated crystals.

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Acknowledgements

This work was supported by the Human Frontier Science Foundation (grant RGP0052/2012), the Deutsche Forschungsgemeinschaft (grants SCHU 1080/12-1 and 15-1) and the European Union (Bio2MaN4MRI). The authors thank F. Kiemer for expert help with iron measurements and cultivation experiments.

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I.K., D.S., Y.Z., Q.T., C.J. and R.M. planned and performed cloning experiments. I.K. and A.L. performed genetic transfers and cultivation experiments. G.W. prepared cryo- and chemically fixed cells. S.B., O.R. and G.W. performed TEM and I.K. analysed the data. J.P. and O.R. performed cryo-electron tomography experiments. E.T. and M.P. took high-resolution TEM micrographs and analysed the data. I.K. and A.L. took fluorescence micrographs and performed phenotypization experiments. I.K. performed western blot experiments and analysed proteomic data. A.B. performed Illumina genome sequencing and I.K. analysed the data. I.K. and D.S. designed the study and wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Youming Zhang or Dirk Schüler.

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Competing interests

I.K. and D.S. (LMU Munich) have filed a patent application on the process described in this work (Production of magnetic nanoparticles in recombinant host cells, EP13193478).

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Kolinko, I., Lohße, A., Borg, S. et al. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nature Nanotech 9, 193–197 (2014). https://doi.org/10.1038/nnano.2014.13

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