The quantitative basis for the redistribution of immobile bacterial lipoproteins to division septa

• Main Authors: Connolley, L. (Author), Kleanthous, C. (Author), Murray, S.M (Author), Szczepaniak, J. (Author)
• Format: Article
• Language: English
• Published: Public Library of Science 2021
• Subjects: Article; bacterial cell wall; bacterial outer membrane; Bacterial Outer Membrane Proteins; bacterial protein; cell division; Cell Division; cell wall; Cell Wall; chemistry; controlled study; cytology; dissociation; Escherichia coli; Escherichia coli protein; Escherichia coli Proteins; ExcC protein, E coli; inner membrane; intracellular space; Intracellular Space; lipoprotein; Lipoproteins; mathematical model; membrane transport; metabolism; mutant; outer membrane protein; peptidoglycan; Peptidoglycan; periplasmic protein; Periplasmic Proteins; phenotype; physiology; prediction; protein binding; Protein Binding; protein localization; protein Pal; protein TolB; protein transport; Protein Transport; proton motive force; quantitative analysis; tolB protein, E coli; unclassified drug
• Online Access: View Fulltext in Publisher

 The spatial localisation of proteins is critical for most cellular function. In bacteria, this is typically achieved through capture by established landmark proteins. However, this requires that the protein is diffusive on the appropriate timescale. It is therefore unknown how the localisation of effectively immobile proteins is achieved. Here, we investigate the localisation to the division site of the slowly diffusing lipoprotein Pal, which anchors the outer membrane to the cell wall of Gram-negative bacteria. While the proton motive force-linked TolQRAB system is known to be required for this repositioning, the underlying mechanism is unresolved, especially given the very low mobility of Pal. We present a quantitative, mathematical model for Pal relocalisation in which dissociation of TolB-Pal complexes, powered by the proton motive force across the inner membrane, leads to the net transport of Pal along the outer membrane and its deposition at the division septum. We fit the model to experimental measurements of protein mobility and successfully test its predictions experimentally against mutant phenotypes. Our model not only explains a key aspect of cell division in Gram-negative bacteria, but also presents a physical mechanism for the transport of low-mobility proteins that may be applicable to multi-membrane organelles, such as mitochondria and chloroplasts. Copyright: © 2021 Connolley et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.