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Cited by 5Bacterial Genetics and BiotechnologyBiochemical and Structural CharacterizationEscherichia coli research studies

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A dynamic bactofilin cytoskeleton cooperates with an M23 endopeptidase to control bacterial morphogenesis

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Pöhl, Sebastian, Osorio-Valeriano, Manuel, Cserti, Emöke, Harberding, Jannik, Hernandez-Tamayo, Rogelio, Biboy, Jacob, Sobetzko, Patrick, Vollmer, Waldemar, Graumann, Peter L, Thanbichler, Martin·2024·eLife
DOI 10.7554/elife.86577PMC PMC10945521

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Abstract

Bactofilins have emerged as a widespread family of cytoskeletal proteins with important roles in bacterial morphogenesis, but their precise mode of action is still incompletely understood. In this study, we identify the bactofilin cytoskeleton as a key regulator of cell growth in the stalked budding alphaproteobacterium Hyphomonas neptunium . We show that, in this species, bactofilin polymers localize dynamically to the stalk base and the bud neck, with their absence leading to unconstrained growth of the stalk and bud compartments, indicating a central role in the spatial regulation of cell wall biosynthesis. Database searches reveal that bactofilin genes are often clustered with genes for cell wall hydrolases of the M23 peptidase family, suggesting a functional connection between these two types of proteins. In support of this notion, we find that the H. neptunium M23 peptidase homolog LmdC interacts directly with bactofilin in vitro and is required for proper cell shape in vivo. Complementary studies in the spiral-shaped alphaproteobacterium Rhodospirillum rubrum again reveal a close association of its bactofilin and LmdC homologs, which co-localize at the inner curve of the cell, modulating the degree of cell curvature. Collectively, these findings demonstrate that bactofilins and M23 peptidases form a conserved functional module that promotes local changes in the mode of cell wall biosynthesis, thereby driving cell shape determination in morphologically complex bacteria.

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Metadata

Authors
Pöhl, S., Osorio-Valeriano, M., Cserti, E., Harberding, J., Hernandez-Tamayo, R., Biboy, J., Sobetzko, P., Vollmer, W., Graumann, P. L., & Thanbichler, M.
Affiliations
  • Philipps University of Marburg (DE)
  • Department of Biology, University of Marburg, Marburg, Germany
  • Max Planck Institute for Terrestrial Microbiology
  • Newcastle University (GB)
  • Loewe Center for Synthetic Microbiology (DE)
  • The University of Queensland (AU)
Corresponding author
Thanbichler, Martin
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2024-01-31
Volume
12
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.86577
PMC
PMC10945521
OpenAlex
W4367054809
Cited by
5
References
1
Citations by year
2025: 2 · 2024: 3
FWCI
0.83
Type
journal article
Language
en
Update notices
correction (2024-07-04)
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • University of Marburg (Core funding)
  • Max-Planck-Gesellschaft (Max Planck Fellowship, PhD fellowship of the IMPRS for Environmental, Cellular and Molecular Microbiology)
  • Deutsche Forschungsgemeinschaft (450420164, 26942323 - TRR 174)
  • Biotechnology and Biological Sciences Research Council (BB/W013630/1)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
  • Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
Keywords
bactofilin, bacterial cytoskeleton, bacterial morphogenesis, Rhodospirillum rubrum, cell shape determination, cell wall biosynthesis, cell wall hydrolases, Alphaproteobacteria, protein-protein interaction
MeSH terms
Bacteria, Bacterial Proteins, Cytoskeletal Proteins, Cytoskeleton, Endopeptidases

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