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

Author:

Pöhl Sebastian1,Osorio-Valeriano Manuel12,Cserti Emöke1,Harberding Jannik1,Hernández-Tamayo Rogelio234,Biboy Jacob5ORCID,Sobetzko Patrick4,Vollmer Waldemar56ORCID,Graumann Peter L.34,Thanbichler Martin124ORCID

Affiliation:

1. Department of Biology, University of Marburg

2. Max Planck Institute for Terrestrial Microbiology

3. Department of Chemistry, University of Marburg

4. Center for Synthetic Microbiology (SYNMIKRO)

5. Centre for Bacterial Cell Biology, Biosciences Institute, Newcastle University

6. Institute for Molecular Bioscience, The University of Queensland

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 in a range of different species bactofilin genes are 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.

Publisher

eLife Sciences Publications, Ltd

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