A cell wall synthase accelerates plasma membrane partitioning in mycobacteria
Abstract
Lateral partitioning of proteins and lipids shapes membrane function. In model membranes, partitioning can be influenced both by bilayer-intrinsic factors like molecular composition and by bilayer-extrinsic factors such as interactions with other membranes and solid supports. While cellular membranes can departition in response to bilayer-intrinsic or -extrinsic disruptions, the mechanisms by which they partition de novo are largely unknown. The plasma membrane of Mycobacterium smegmatis spatially and biochemically departitions in response to the fluidizing agent benzyl alcohol, then repartitions upon fluidizer washout. By screening for mutants that are sensitive to benzyl alcohol, we show that the bifunctional cell wall synthase PonA2 promotes membrane partitioning and cell growth during recovery from benzyl alcohol exposure. PonA2's role in membrane repartitioning and regrowth depends solely on its conserved transglycosylase domain. Active cell wall polymerization promotes de novo membrane partitioning and the completed cell wall polymer helps to maintain membrane partitioning. Our work highlights the complexity of membrane-cell wall interactions and establishes a facile model system for departitioning and repartitioning cellular membranes.
Data availability
Sequencing data have been deposited in NIH SRA under accession codes PRJNA976743.All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for all Figures and figure supplements.
Article and author information
Author details
Funding
National Institute of Allergy and Infectious Diseases (R21 AI144748)
- Yasu S Morita
National Institute of Allergy and Infectious Diseases (R21 AI144748)
- M Sloan Siegrist
National Institute of Allergy and Infectious Diseases (DP2 AI138238)
- M Sloan Siegrist
National Institute of Allergy and Infectious Diseases (R03 AI140259-01)
- Yasu S Morita
National Institute of General Medical Sciences (R35GM143057)
- Enrique R Rojas
National Institute of General Medical Sciences (T32 GM008515)
- Emily S Melzer
Uehara Memorial Foundation
- Takehiro Kado
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Petra Anne Levin, Washington University in St. Louis, United States
Version history
- Preprint posted: June 14, 2022 (view preprint)
- Received: July 16, 2022
- Accepted: September 2, 2023
- Accepted Manuscript published: September 4, 2023 (version 1)
- Version of Record published: October 3, 2023 (version 2)
Copyright
© 2023, Kado et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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