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Exploring the host range for genetic transfer of magnetic organelle biosynthesis

Nature Nanotechnology volume 19, pages 115–123 (2024)Cite this article

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Abstract

Magnetosomes produced by magnetotactic bacteria have great potential for application in biotechnology and medicine due to their unique physicochemical properties and high biocompatibility. Attempts to transfer the genes for magnetosome biosynthesis into non-magnetic organisms have had mixed results. Here we report on a systematic study to identify key components needed for magnetosome biosynthesis after gene transfer. We transfer magnetosome genes to 25 proteobacterial hosts, generating seven new magnetosome-producing strains. We characterize the recombinant magnetosomes produced by these strains and demonstrate that denitrification and anaerobic photosynthesis are linked to the ability to synthesize magnetosomes upon the gene transfer. In addition, we show that the number of magnetosomes synthesized by a foreign host negatively correlates with the guanine–cytosine content difference between the host and the gene donor. Our findings have profound implications for the generation of magnetized living cells and the potential for transgenic biogenic magnetic nanoparticle production.

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Fig. 1: Experimental strategy used to survey bacterial hosts for heterologous magnetosome production.
Fig. 2: Overview of the magnetosome-producing hosts.
Fig. 3: Crystallographic analysis of the magnetosomes produced by C. sphaeroides MAG and Rhodopseudomonas pseudopalustris MAG.
Fig. 4: Crystallographic analysis of the magnetosomes produced by Rhodomicrobium vannielii MAG.
Fig. 5: Impact of pH on the magnetosome biosynthesis in Rhodoblastus acidophilus MAG.
Fig. 6: Genome–genome comparisons of M+ and M– strains.

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Data availability

The dataset used for the comparative analysis of the orthologues across the genomes is deposited to the following repository together with the tidy data and the code for the analysis: https://github.com/MarDZiuba/pangenomemtx_to_Venn. Sequencing reads originating from this study were deposited to NCBI GenBank under the BioProject number PRJNA923495. Source data are provided with this paper.

Code availability

The script used to compare the orthologues and visualize the result is available at https://github.com/MarDZiuba/pangenomemtx_to_Venn.git. The script used to parse the magnetosome size measurements and generate the violin plots can be accessed at https://github.com/MarDZiuba/magsizeplot.git.

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Acknowledgements

This study was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant no. 692637 to D.S.). We are grateful to M. Schüler and S. Geimer for their help with electron microscopy. Electron microscopy performed at University of Pannonia was supported by the National Research, Development and Innovation Office (Hungary; grant no. RRF-2.3.1-21-2022-00014 to M.P.). We also thank A. Hübner, L. Borgert, J. Kachel and B. Melzer for technical assistance.

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Authors and Affiliations

  1. Department of Microbiology, Faculty of Biology, Chemistry and Geosciences, University of Bayreuth, Bayreuth, Germany

    Marina V. Dziuba, Frank-Dietrich Müller & Dirk Schüler

  2. ELKH-PE Environmental Mineralogy Research Group, Veszprém, Hungary

    Mihály Pósfai

  3. Research Institute of Biomolecular and Chemical Engineering, University of Pannonia, Veszprém, Hungary

    Mihály Pósfai

Authors
  1. Marina V. Dziuba
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  2. Frank-Dietrich Müller
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Contributions

D.S. and M.V.D. conceived, conceptualized and designed the experiments. M.V.D. performed the experiments, measurements and data analyses. F.-D.M. conducted the magnetosome gene transfer to Rhodomicrobium vannielii and analysed the phenotype in the strain. M.P. carried out the crystallography analysis. M.V.D. and D.S. wrote the original draft along with review and editing. D.S. carried out the funding acquisition, project administration and supervision. All authors discussed the results and commented on the manuscript.

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Correspondence to Dirk Schüler.

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Nature Nanotechnology thanks Donna Goldhawk and Jie Tian for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Crystallographic analysis of the magnetosomes produced by B. viridis MAG.

(a) and (e) BF TEM micrographs of the magnetosome chain. HAADF image (b) and elemental maps (c, d-i) of the boxed area in (a). (d-ii) EDS spectra of the areas marked in (d-i), indicating that flake-like particles also contain Fe and O. (f) HRTEM image of the magnetosome chain from the boxed area in (e) with FFT of the twinned particle in the center, with one of its parts in [112] zone-axis orientation of magnetite.

Extended Data Fig. 2 Crystallographic analysis of the magnetosomes produced by Rhodoblastus acidophilus MAG.

(a) BF TEM micrograph of the cells. (b) HAADF image of the boxed area in (a) with (c–e) close-up HAADF image and elemental maps of the boxed region in (b). (e-ii) EDS spectra of the areas marked in (e-i). Fe-O-P-rich particles in area #1 likely represent ferrosomes, whereas particles in area #2 are magnetite magnetosomes. (f) and (g) HRTEM images with FFTs of the indicated particles. The particle in (f) and the lower, small particle in (g) are magnetite in [130] and [110] zone-axis orientations, respectively, whereas the upper particle in (g) is amorphous (a putative ferrosome).

Extended Data Fig. 3 Crystallographic analysis of the magnetosomes produced by A. brasilense MAG.

(a) BF TEM micrograph of the cells with magnetosomes. (b) HRTEM image of the magnetosomes from the boxed area in (a) with FFTs of the magnetosomes in zone-axis orientations consistent with magnetite. (c) EDS spectrum of the magnetosome marked with an asterisk in (b). (d-f) HAADF image and elemental maps of the magnetosome chain.

Supplementary information

Supplementary Information

Supplementary Figs. 1–6 and Tables 1–4.

Reporting Summary

Supplementary Video 1

Magnetic response of Rhodomicrobium vannielii MAG culture.

Source data

Source Data Fig. 2

Magnetosome diameter measurements (in nanometres) for all magnetized strains and M. gryphiswaldense, used to create the violin plot in Fig. 2h, along with the statistical summary of the data.

Source Data Fig. 4

Source data for Fig. 4a–d: OD660, Cmag values, magnetosome numbers per cell and diameter measurements (in nanometres).

Source Data Fig. 6

G+C% differences between the strains calculated using whole genomes along with magnetosome core diameters (as in Source Data Fig. 2h) and magnetosome numbers per cell.

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Dziuba, M.V., Müller, FD., Pósfai, M. et al. Exploring the host range for genetic transfer of magnetic organelle biosynthesis. Nat. Nanotechnol. 19, 115–123 (2024). https://doi.org/10.1038/s41565-023-01500-5

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