Contributions of Membrane Lipids to Bacterial Cell Homeostasis upon Osmotic Challenge
Changing environmental osmotic pressure causes transmembrane water fluxes that may impair cellular functions. Bacteria mitigate water fluxes by controlling the solute content of their cytoplasm. Increasing osmotic pressure triggers solute synthesis or uptake via osmosensing transporters, whereas osmotic downshock triggers solute release via mechanosensitive channels. Membrane lipids are implicated in the subcellular localization and function of membrane-based osmoregulatory systems. Zwitterionic phosphatidylethanolamine (PE) and anionic phosphatidylglycerol (PG) and cardiolipin (CL) are the predominant phospholipids in most bacteria, but their proportions vary widely. For many species, anionic lipids increase in proportion during cultivation in high salinity media. Evidence suggests that interactions among anionic lipid headgroups and cytoplasm-exposed areas of osmosensory transporters ProP, BetP, and OpuA are fundamental to their osmosensory response. CL-dependent targeting of transporter ProP to the CL-rich environment at the poles of Escherichia coli cells further modulates the osmolality response. Protein-lipid interactions are also fundamental to the gating of mechanosensitive channels MscL and MscS by membrane tension. Future work should encompass further characterization of the impacts of lipid composition on key physical properties of the membrane, as well as the regulation of lipid composition and membrane properties in response to environmental cues. The roles of lipids in the structural mechanisms of osmosensing and mechanosensitive channel gating are not fully understood. Osmosensory systems provide useful paradigms for the study of both protein-lipid interactions and the role of subcellular localization in bacterial lipid and protein function.
The authors are grateful for helpful discussions with Ronald N. McElhaney (University of Alberta), Robert S. Hodges (University of Colorado), Kerwyn C. Huang (Stanford University), Tariq Akhtar and Leonid Brown (University of Guelph), and members of the Wood laboratory. We also thank the Natural Sciences and Engineering Research Council of Canada and the Canadian Institutes for Health Research for financial support.
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