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Bdellovibrio predation cycle characterized at nanometre-scale resolution with cryo-electron tomography

Nature Microbiology volume 8, pages 1267–1279 (2023)Cite this article

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Abstract

Bdellovibrio bacteriovorus is a microbial predator that offers promise as a living antibiotic for its ability to kill Gram-negative bacteria, including human pathogens. Even after six decades of study, fundamental details of its predation cycle remain mysterious. Here we used cryo-electron tomography to comprehensively image the lifecycle of B. bacteriovorus at nanometre-scale resolution. With high-resolution images of predation in a native (hydrated, unstained) state, we discover several surprising features of the process, including macromolecular complexes involved in prey attachment/invasion and a flexible portal structure lining a hole in the prey peptidoglycan that tightly seals the prey outer membrane around the predator during entry. Unexpectedly, we find that B. bacteriovorus does not shed its flagellum during invasion, but rather resorbs it into its periplasm for degradation. Finally, following growth and division in the bdelloplast, we observe a transient and extensive ribosomal lattice on the condensed B. bacteriovorus nucleoid.

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Fig. 1: Anatomy of attack-phase B. bacteriovorus.
Fig. 2: Attachment of B. bacteriovorus to prey.
Fig. 3: B. bacteriovorus flagellar absorption.
Fig. 4: B. bacteriovorus prey invasion.
Fig. 5: Anatomy of the bdelloplast.
Fig. 6: Ribosomal nucleoid lattice in the end-stage bdelloplast.

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Data availability

The full tomograms are available upon request.

Code availability

A tutorial (containing the codes) is available demonstrating how to use VISFD to segment tomograms of B. bacteriovorus cells (see jewettaij/visfd_tutorials: updated ‘STEP_0’ of the Bdellovibrio segmentation example (2021) https://doi.org/10.5281/ZENODO.5758691).

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Acknowledgements

This project was funded by the National Institutes of Health (grant R01 AI127401 to G.J.J.) and a Baxter postdoctoral fellowship from Caltech to M.K. S.K. is supported by the Swedish Research Council (2019-06293). Cryo-ET work was performed in the Beckman Institute Resource Center for Transmission Electron Microscopy at the California Institute of Technology and the Howard Hughes Medical Institute Janelia Farm CryoEM Facility. We thank D. Villanueva Avalos for making the summary animation. We are deeply grateful to L. Sockett (University of Nottingham) for the gift of the B. bacteriovorus strain and helpful advice and comments.

Author information

Author notes

  1. Mohammed Kaplan

    Present address: Department of Microbiology, University of Chicago, Chicago, IL, USA

  2. Yi-Wei Chang

    Present address: Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

  3. These authors contributed equally: Mohammed Kaplan, Yi-Wei Chang.

Authors and Affiliations

  1. Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA

    Mohammed Kaplan, Yi-Wei Chang, Catherine M. Oikonomou, William J. Nicolas, Stefan Kreida, Przemysław Dutka, Stefano Maggi & Grant J. Jensen

  2. Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA, USA

    Andrew I. Jewett

  3. Department of Microbiology, Tumor and Cell Biology, Karolinska Institute, Solna, Sweden

    Stefan Kreida

  4. Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena, CA, USA

    Przemysław Dutka

  5. Howard Hughes Medical Institute, Pasadena, CA, USA

    Lee A. Rettberg

  6. Department of Chemistry and Biochemistry, Brigham Young University, Provo, UT, USA

    Grant J. Jensen

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Contributions

M.K., Y.-W.C. and G.J.J. conceived the project. M.K. and Y.-W.C. collected the data. M.K., L.A.R., S.K. and Y.-W.C. prepared samples. W.J.N. and A.I.J. performed tomogram segmentations. S.M. performed the PCA of T4P. P.D. performed the ribosome subtomogarm averaging and helped in the data visualization and analysis relative to the ribosome averages. M.K., C.M.O., Y.-W.C., A.I.J., L.A.R. and G.J.J. performed data analysis. M.K. wrote the original manuscript, which was first edited by C.M.O. and G.J.J., then all authors read and further edited the manuscript.

Corresponding authors

Correspondence to Mohammed Kaplan or Grant J. Jensen.

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Nature Microbiology thanks Andrew Lovering, Andrew Fenton and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Supplementary Figs. 1-43 and Tables 1 and 2.

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Supplementary Video 1

An electron cryo-tomogram of an attack-phase B. bacteriovorus cell highlighting limited arrangement of ribosomes on some parts of the surface of the compacted nucleoid. Note the flagellum and chemosensory array at one pole and T4aP at the opposite pole. Scale bar, 100 nm.

Supplementary Video 2

An electron cryo-tomogram of an attack-phase B. bacteriovorus cell highlighting the presence of two 8-nm-wide cytoplasmic tubes. Scale bar, 100 nm. Note that these tubes are usually located at different heights inside a cell; hence, it is more probable to see one tube instead of two in a 2D slice through a 3D tomogram at a certain z-level as in Supplementary Fig. 2. Scale bar, 100 nm.

Supplementary Video 3

An electron cryo-tomogram highlighting T4aP extending from a B. bacteriovorus cell to the OM of an E. coli minicell. Scale bar, 100 nm.

Supplementary Video 4

An electron cryo-tomogram highlighting T4aP extending from a B. bacteriovorus cell to the OM of an E. coli minicell. Scale bar, 100 nm.

Supplementary Video 5

An electron cryo-tomogram of a B. bacteriovorus cell in close proximity to an E. coli minicell indicating the presence of multiple rose-like complexes and non-piliated T4aP basal bodies at the contact site. Scale bar, 100 nm.

Supplementary Video 6

An electron cryo-tomogram of a B. bacteriovorus cell attached to an E. coli minicell and accompanying 3D segmentation. An attachment plaque and T4aP basal bodies (blue cylinders) can be seen at the biting pole, while an early stage of flagellar resorption can be seen at the other pole. Scale bar, 100 nm.

Supplementary Video 7

An electron cryo-tomogram of a B. bacteriovorus cell attached to an E. coli minicell and accompanying 3D segmentation. An attachment plaque, rose-like complexes (light green) and T4aP basal bodies (blue cylinders) can be seen at the biting pole, while an intermediate stage of flagellar absorption into the periplasm can be seen at the other pole. Scale bar, 100 nm.

Supplementary Video 8

An electron cryo-tomogram of a B. bacteriovorus cell attached to an E. coli minicell and accompanying segmentation. An attachment plaque and T4aP basal bodies (blue cylinders) can be seen at the biting pole, while a late stage of flagellar resorption can be seen at the other pole. The broken periplasmic flagellar filament is wrapped around the cell. Scale bar, 100 nm.

Supplementary Video 9

An electron cryo-tomogram of a B. bacteriovorus cell attached to an E. coli minicell by an attachment plaque. A late stage of flagellar resorption can be seen at the other pole with the periplasmic flagellar filament wrapping around the cell. Scale bar, 50 nm.

Supplementary Video 10

An electron cryo-tomogram of a B. bacteriovorus cell attached to an E. coli minicell with an attachment plaque. A late stage of flagellar resorption can be seen where the exit hole of the flagellum is far from the motor and a notable part of the flagellar filament is in the periplasm. Scale bar, 50 nm.

Supplementary Video 11

An electron cryo-tomogram of two B. bacteriovorus cells, one of them attached to an E. coli minicell with an attachment plaque. A late stage of flagellar resorption can be seen with the periplasmic flagellar filament wrapping around the cell. No flagellar motor could be identified in this cryo-tomogram. Scale bar, 50 nm.

Supplementary Video 12

An electron cryo-tomogram of a non-productive invasion by a B. bacteriovorus cell of an E. coli minicell. A portal can be seen surrounding the entry hole, and many vesicles are present inside the prey. Scale bar, 100 nm.

Supplementary Video 13

An electron cryo-tomogram of an end-stage non-productive invasion by a B. bacteriovorus cell of an E. coli minicell, in which all the prey cytoplasm has been consumed. A portal with associated membrane blebs can be seen at the entry hole. The ribosomes exhibit a regular hexagonal packing around much of the nucleoid surface. Scale bar, 100 nm.

Supplementary Video 14

An electron cryo-tomogram showing a B. bacteriovorus cell near a lysed E. coli minicell. Multiple knob-like densities can be seen at one pole of the B. bacteriovorus cell (highlighted by white arrows). Scale bar, 100 nm.

Supplementary Video 15

An electron cryo-tomogram of an E. coli bdelloplast, and accompanying 3D segmentation, highlighting the tentative seal at the entry hole. A substantial part of the prey’s cytoplasm is still present. Scale bar, 100 nm.

Supplementary Video 16

An electron cryo-tomogram of a V. cholerae bdelloplast highlighting multiple uniformly sized vesicles inside the bdelloplast. A substantial part of the prey’s cytoplasm is still present. Scale bar, 50 nm.

Supplementary Video 17

An electron cryo-tomogram of a V. cholerae bdelloplast, and a segmentation thereof, containing two newly divided B. bacteriovorus cells highlighting the bdelloplast tentative seal and prey flagellar relic. Inside the bdelloplast, uniformly sized vesicles and a dense sphere of yet-undigested prey cytoplasm are present. Scale bar, 100 nm.

Supplementary Video 18

An electron cryo-tomogram of an end-stage E. coli minicell bdelloplast highlighting the tentative seal, multiple uniformly sized vesicles and ribosomes in a regular hexagonal arrangement on the nucleoid surface. Scale bar, 100 nm.

Supplementary Video 19

An electron cryo-tomogram of an end-stage E. coli minicell bdelloplast highlighting multiple uniformly sized vesicles and a hexagonal lattice of ribosomes around the nucleoid. No prey cytoplasm remains. Scale bar, 100 nm.

Supplementary Video 20

An electron cryo-tomogram of an end-stage E. coli minicell bdelloplast highlighting multiple uniformly sized vesicles and a hexagonal lattice of ribosomes around the nucleoid. No prey cytoplasm remains. Scale bar, 100 nm.

Supplementary Video 21

An electron cryo-tomogram of an end-stage E. coli minicell bdelloplast containing two newly divided B. bacteriovorus cells and accompanying segmentation. No prey cytoplasm remains, and many ribosomes can be seen regularly arranged around the nucleoids of the two predator cells. Scale bar, 100 nm.

Supplementary Video 22

An electron cryo-tomogram of a B. bacteriovorus cell associated with a lysed E. coli minicell and accompanying segmentation, highlighting the regular arrangement of many ribosomes around the nucleoid. Scale bar, 100 nm.

Supplementary Video 23

A summary of the predatory lifecycle of B. bacteriovorus based on the in situ cryo-ET data presented in this study.

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Kaplan, M., Chang, YW., Oikonomou, C.M. et al. Bdellovibrio predation cycle characterized at nanometre-scale resolution with cryo-electron tomography. Nat Microbiol 8, 1267–1279 (2023). https://doi.org/10.1038/s41564-023-01401-2

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