Abstract
The ability to produce outer membrane projections in the form of tubular membrane extensions (MEs) and membrane vesicles (MVs) is a widespread phenomenon among diderm bacteria. Despite this, our knowledge of the ultrastructure of these extensions and their associated protein complexes remains limited. Here, we surveyed the ultrastructure and formation of MEs and MVs, and their associated protein complexes, in tens of thousands of electron cryo-tomograms of ~90 bacterial species that we have collected for various projects over the past 15 years (Jensen lab database), in addition to data generated in the Briegel lab. We identified outer MEs and MVs in 13 diderm bacterial species and classified several major ultrastructures: (1) tubes with a uniform diameter (with or without an internal scaffold), (2) tubes with irregular diameter, (3) tubes with a vesicular dilation at their tip, (4) pearling tubes, (5) connected chains of vesicles (with or without neck-like connectors), (6) budding vesicles and nanopods. We also identified several protein complexes associated with these MEs and MVs which were distributed either randomly or exclusively at the tip. These complexes include a secretin-like structure and a novel crown-shaped structure observed primarily in vesicles from lysed cells. In total, this work helps to characterize the diversity of bacterial membrane projections and lays the groundwork for future research in this field.
Original language | English |
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Article number | e73099 |
Journal | eLife |
Volume | 10 |
DOIs | |
State | Published - Sep 2021 |
Bibliographical note
Publisher Copyright:© Kaplan et al.
Funding
This project was funded by the NIH (grant R35 GM122588 to GJJ, and P20 GM130456 to CLS) and a Baxter postdoctoral fellowship from Caltech to MK. Cryo-ET work was done in the Beckman Institute Resource Center for Transmission Electron Microscopy at the California Institute of Technology. We are grateful to Prof. Martin Pilhofer for collecting the P. luteoviolacea data and for critically reading the manuscript. We thank Prof. Elitza I Tocheva for collecting the D. acidovorans data. We thank Prof. Mohamed El-Naggar for insights into preparing S. oneidensis samples and Dr. Yuxi Liu for discussions. Briegel lab data was collected at the Netherlands Center for Electron Nanoscopy with support from Dr Wen Yang. This data was collected with support from the National Roadmap for Large-Scale Research Infrastructure 2017–2018 with project number 184.034.014, which is financed in part by the Dutch Research Council (NWO). This work was also supported by the NWO OCENW. GROOT.2019.063 grant.
Funders | Funder number |
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NWO OCENW | |
National Institutes of Health (NIH) | R35 GM122588, 184.034.014 |
National Institutes of Health (NIH) | |
National Institute of General Medical Sciences | P20GM130456 |
National Institute of General Medical Sciences | |
Nederlandse Organisatie voor Wetenschappelijk Onderzoek |
ASJC Scopus subject areas
- General Neuroscience
- General Biochemistry, Genetics and Molecular Biology
- General Immunology and Microbiology