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Contributions of Membrane Lipids to Bacterial Cell Homeostasis upon Osmotic Challenge

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Book cover Biogenesis of Fatty Acids, Lipids and Membranes

Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

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Abstract

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.

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References

  • Agmo Hernández V, Eriksson EK, Edwards K (2015) Ubiquinone-10 alters mechanical properties and increases stability of phospholipid membranes. Biochim Biophys Acta 1848:2233–2243

    Article  PubMed  CAS  Google Scholar 

  • Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci U S A 111:7898–7905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barak I, Muchova K (2013) The role of lipid domains in bacterial cell processes. Int J Mol Sci 14:4050–4065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barák I, Muchová K, Wilkinson AJ, O’Toole PJ, Pavlendová N (2008) Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 68:1315–1327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Battle AR, Ridone P, Bavi N, Nakayama Y, Nikolaev YA, Martinac B (2015) Lipid–protein interactions: lessons learned from stress. Biochim Biophys Acta 1848:1744–1756

    Article  CAS  PubMed  Google Scholar 

  • Benesch MGK, Lewis RNAH, McElhaney RN (2015) On the miscibility of cardiolipin with 1,2-diacyl phosphoglycerides: binary mixtures of dimyristoylphosphatidylglycerol and tetramyristoylcardiolipin. Biochim Biophys Acta 1848:2878–2888

    Article  CAS  PubMed  Google Scholar 

  • Bialecka-Fornal M, Lee HJ, DeBerg HA, Gandhi CS, Phillips R (2012) Single-cell census of mechanosensitive channels in living bacteria. PLoS One 7:e33077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bialecka-Fornal M, Lee HJ, Phillips R (2015) The rate of osmotic downshock determines the survival probability of bacterial mechanosensitive channel mutants. J Bacteriol 197:231–237

    Article  PubMed  CAS  Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  CAS  PubMed  Google Scholar 

  • Boekema EJ, Scheffers DJ, van Bezouwen LS, Bolhuis H, Folea IM (2013) Focus on membrane differentiation and membrane domains in the prokaryotic cell. J Mol Microbiol Biotechnol 23:345–356

    Article  CAS  PubMed  Google Scholar 

  • Booth IR, Blount P (2012) The MscS and MscL families of mechanosensitive channels act as microbial emergency release valves. J Bacteriol 194:4802–4809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boucher PA, Morris CE, Joos B (2009) Mechanosensitive closed-closed transitions in large membrane proteins: osmoprotection and tension damping. Biophys J 97:2761–2770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bramkamp M, Lopez D (2015) Exploring the existence of lipid rafts in bacteria. Microbiol Mol Biol Rev 79:81–100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown GR, Sutcliffe IC, Bendell D, Cummings SP (2000) The modification of the membrane of Oceanomonas baumannii when subjected to both osmotic and organic solvent stress. FEMS Microbiol Lett 189:149–154

    Article  CAS  PubMed  Google Scholar 

  • Brown GR, Sutcliffe IC, Cummings SP (2003) Combined solvent and water activity stresses on turgor regulation and membrane adaptation in Oceanimonas baumannii ATCC 700832. Antonie Van Leeuwenhoek 83:275–283

    Article  CAS  PubMed  Google Scholar 

  • Busiek KK, Margolin W (2015) Bacterial actin and tubulin homologs in cell growth and division. Curr Biol 25:R243–R254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catucci L, Depalo N, Lattanzio VMT, Agostiano A, Corcelli, A (2004) Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochem 43:15066–15072.

    Article  CAS  Google Scholar 

  • Cronan JE (2003) Bacterial membrane lipids: where do we stand? Annu Rev Microbiol 57:203–224

    Article  CAS  PubMed  Google Scholar 

  • Culham DE, Meinecke M, Wood JM (2012) Impacts of the osmolality and the lumenal ionic strength on osmosensory transporter ProP in proteoliposomes. J Biol Chem 287:27813–27822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Culham DE, Shkel IA, Record MT, Wood JM (2016) Contributions of Coulombic and Hofmeister effects to the osmotic activation of Escherichia coli transporter ProP. Biochemistry 55:1301–1313

    Article  CAS  PubMed  Google Scholar 

  • Danevcic T, Rilfors L, Strancar J, Lindblom G, Stopar D (2005) Effects of lipid composition on the membrane activity and lipid phase behaviour of Vibrio sp. DSM14379 cells grown at various NaCl concentrations. Biochim Biophys Acta 1712:1–8

    Article  CAS  PubMed  Google Scholar 

  • Dare K, Shepherd J, Roy H, Seveau S, Ibba M (2014) LysPGS formation in Listeria monocytogenes has broad roles in maintaining membrane integrity beyond antimicrobial peptide resistance. Virulence 5:534–546

    Article  PubMed  PubMed Central  Google Scholar 

  • de Wit G, Danial JSH, Kukura P, Wallace MI (2015) Dynamic label-free imaging of lipid nanodomains. Proc Natl Acad Sci U S A 112:12299–12303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edwards MD, Black S, Rasmussen T, Rasmussen A, Stokes NR, Stephen T-L, Miller S, Booth IR (2012) Characterization of three novel mechanosensitive channel activities in Escherichia coli. Channels 6:272–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fishov I, Norris V (2012) Membrane heterogeneity created by transertion is a global regulator in bacteria. Curr Opin Microbiol 15:724–730

    Article  CAS  PubMed  Google Scholar 

  • Fishov I, Woldringh C (1999) Visualization of membrane domains in Escherichia coli. Mol Microbiol 32:1166–1172

    Article  CAS  PubMed  Google Scholar 

  • Frias M, Benesch MGK, Lewis RNAH, McElhaney RN (2011) On the miscibility of cardiolipin with 1,2-diacyl phosphoglycerides: binary mixtures of dimyristoylphosphatidylethanolamine and tetramyristoylcardiolipin. Biochim Biophys Acta 1808:774–783

    Article  CAS  PubMed  Google Scholar 

  • Gennis RB (1989) Biomembranes: molecular structure and function. Springer, New York

    Book  Google Scholar 

  • Gill RL, Castaing J-P, Hsin J, Tan IS, Wang X, Huang KC, Tian F, Ramamurthi KS (2015) Structural basis for the geometry-driven localization of a small protein. Proc Natl Acad Sci 112:E1908–E1915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Govindarajan S, Elisha Y, Nevo-Dinur K, Amster-Choder O (2013) The general phosphotransferase system proteins localize to sites of strong negative curvature in bacterial cells. mBio 4:00443-13

    Google Scholar 

  • Grage SL, Keleshian AM, Turdzeladze T, Battle AR, Tay WC, May RP, Holt SA, Contera SA, Haertlein M, Moulin M et al (2011) Bilayer-mediated clustering and functional interaction of MscL channels. Biophys J 100:1252–1260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffin BA, Adams SR, Jones J, Tsien RY (2000) Fluorescent labeling of recombinant proteins in living cells with FlAsH. Methods Enzymol 327:565–578

    Article  CAS  PubMed  Google Scholar 

  • Guillot A, Obis D, Mistou M-Y (2000) Fatty acid membrane composition and activation of glycine-betaine transport in Lactococcus lactis subjected to osmotic stress. Int J Food Microbiol 55:47–51

    Article  CAS  PubMed  Google Scholar 

  • Gul N, Poolman B (2013) Functional reconstitution and osmoregulatory properties of the ProU ABC transporter from Escherichia coli. Mol Membr Biol 30:138–148

    Article  PubMed  Google Scholar 

  • Guler G, Gartner RM, Ziegler C, Mantele W (2015) Lipid-protein interactions in the regulated betaine symporter BetP probed by infrared spectroscopy. J Biol Chem 291:4295–4307

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gullingsrud J, Schulten K (2004) Lipid bilayer pressure profiles and mechanosensitive channel gating. Biophys J 86:3496–3509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Häse CC, Minchin RF, Kloda A, Martinac B (1997) Cross-linking studies and membrane localization and assembly of radiolabelled large mechanosensitive ion channel (MscL) of Escherichia coli. Biochem Biophys Res Commun 232:777–782

    Article  PubMed  Google Scholar 

  • Huang KC, Mukhopadhyay R, Wingreen NS (2006) A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput Biol 2:e151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huijbregts RP, de Kroon AI, de Kruijff B (2000) Topology and transport of membrane lipids in bacteria. Biochim Biophys Acta 1469:43–61

    Article  CAS  PubMed  Google Scholar 

  • Ingólfsson HI, Arnarez C, Periole X, Marrink SJ (2016) Computational ‘microscopy’ of cellular membranes. J Cell Sci 129:257–268

    Article  PubMed  CAS  Google Scholar 

  • Jyothikumar V, Klanbut K, Tiong J, Roxburgh JS, Hunter IS, Smith TK, Herron PR (2012) Cardiolipin synthase is required for Streptomyces coelicolor morphogenesis. Mol Microbiol 84:181–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karasawa A, Erkens GB, Berntsson RPA, Otten R, Schuurman-Wolters GK, Mulder FAA, Poolman B (2011) Cystathionine β-Synthase (CBS) domains 1 and 2 fulfill different roles in ionic strength sensing of the ATP-binding cassette (ABC) transporter OpuA. J Biol Chem 286:37280–37291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karasawa A, Swier LJYM, Stuart MCA, Brouwers J, Helms B, Poolman B (2013) Physicochemical factors controlling the activity and energy coupling of an ionic strength-gated ATP-binding cassette (ABC) transporter. J Biol Chem 288:29862–29871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kates M, Syz JY, Gosser D, Haines TH (1993) pH-dissociation characteristics of cardiolipin and its 2′-deoxy analogue. Lipids 28:877–882

    Article  CAS  PubMed  Google Scholar 

  • Kaurola P, Sharma V, Vonk A, Vattulainen I, Róg T (2016) Distribution and dynamics of quinones in the lipid bilayer mimicking the inner membrane of mitochondria. Biochim Biophys Acta 1858:2116–2122

    Article  CAS  PubMed  Google Scholar 

  • Khakbaz P, Klauda JB (2015) Probing the importance of lipid diversity in cell membranes via molecular simulation. Chem Phys Lipids 192:12–22

    Article  CAS  PubMed  Google Scholar 

  • Koppelman C-M, den Blaauwen T, Duursma MC, Heeren RMA, Nanninga N (2001) Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 183:6144–6147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprowski P, Grajkowski W, Balcerzak M, Filipiuk I, Fabczak H, Kubalski A (2015) Cytoplasmic domain of MscS interacts with cell division protein FtsZ: a possible non-channel function of the mechanosensitive channel in Escherichia coli. PLoS One 10:e0127029

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koshy C, Ziegler C (2015) Structural insights into functional lipid–protein interactions in secondary transporters. Biochim Biophys Acta 1850:476–487

    Article  CAS  PubMed  Google Scholar 

  • Koshy C, Schweikhard ES, Gartner RM, Perez C, Yildiz O, Ziegler C (2013) Structural evidence for functional lipid interactions in the betaine transporter BetP. EMBO J 32:3096–3105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kramer R (2010) Bacterial stimulus perception and signal transduction: response to osmotic stress. Chem Rec 10:217–229

    Article  PubMed  CAS  Google Scholar 

  • Kramer R, Nicklisch S, Ott V (2010) Use of liposomes to study cellular osmosensors. Methods Mol Biol 606:21–30

    Article  PubMed  CAS  Google Scholar 

  • Kusaka J, Shuto S, Imai Y, Ishikawa K, Saito T, Natori K, Matsuoka S, Hara H, Matsumoto K (2016) Septal localization by membrane targeting sequences and a conserved sequence essential for activity at the COOH-terminus of Bacillus subtilis cardiolipin synthase. Res Microbiol 167:202–214

    Article  CAS  PubMed  Google Scholar 

  • Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT, Baldwin AJ, Robinson CV (2014) Membrane proteins bind lipids selectively to modulate their structure and function. Nature 510:172–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai Y-T, Chang Y-Y, Hu L, Yang YH, Chao A, Du Z-Y, Tanner JA, Chye M-L, Qian C, Ng K-M et al (2015) Rapid labeling of intracellular His-tagged proteins in living cells. Proc Natl Acad Sci U S A 112:2948–2953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laloux G, Jacobs-Wagner C (2014) How do bacteria localize proteins to the cell pole? J Cell Sci 127:11–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landgraf D, Okumus B, Chien P, Baker TA, Paulsson J (2013) Segregation of molecules at cell division reveals native protein localization. Nat Methods 9:480–486

    Article  CAS  Google Scholar 

  • Lewis JR, Cafiso DS (1999) Correlation between the free energy of a channel-forming voltage-gated peptide and the spontaneous curvature of bilayer lipids. Biochemistry 38:5932–5938

    Article  CAS  PubMed  Google Scholar 

  • Lewis RNAH, McElhaney RN (2000) Surface charge markedly attenuates the nonlamellar phase-forming propensities of lipid bilayer membranes: calorimetric and 31P-nuclear magnetic resonance studies of mixtures of cationic, anionic, and zwitterionic lipids. Biophys J 79:1455–1464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis RNAH, McElhaney RN (2009) The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes. Biochim Biophys Acta 1788:2069–2079

    Article  CAS  PubMed  Google Scholar 

  • Lin TY, Weibel DB (2016) Organization and function of anionic phospholipids in bacteria. Appl Microbiol Biotechnol 100:4255–4267

    Article  CAS  PubMed  Google Scholar 

  • Lin S-Y, Huang M-Z, Chang H-C, Shiea J (2007) Using electrospray-assisted laser desorption/ionization mass spectrometry to characterize organic compounds separated on thin-layer chromatography plates. Anal Chem 79:8789–8795

    Article  CAS  PubMed  Google Scholar 

  • Lopalco P, Angelini R, Lobasso S, Köcher S, Thompson M, Müller V, Corcelli A (2013) Adjusting membrane lipids under salt stress: the case of the moderate halophilic organism Halobacillus halophilus. Environ Microbiol 15:1078–1087

    Article  CAS  PubMed  Google Scholar 

  • López CS, Heras H, Garda H, Ruzal S, Sánchez-Rivas C, Rivas E (2000) Biochemical and biophysical studies of Bacillus subtilis envelopes under hyperosmotic stress. Int J Food Microbiol 55:137–142

    Article  PubMed  Google Scholar 

  • López CS, Alice AF, Heras H, Rivas EA, Sánchez-Rivas C (2006) Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity. Microbiology 152:605–616

    Article  PubMed  CAS  Google Scholar 

  • Maddock JR, Shapiro L (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259:1717–1723

    Article  CAS  PubMed  Google Scholar 

  • Magalon A, Alberge F (2016) Distribution and dynamics of OXPHOS complexes in the bacterial cytoplasmic membrane. Biochim Biophys Acta 1857:198–213

    Article  CAS  PubMed  Google Scholar 

  • Margolin W (2012) The price of tags in protein localization studies. J Bacteriol 194:6369–6371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsumoto K, Kusaka J, Nishibori A, Hara H (2006) Lipid domains in bacterial membranes. Mol Microbiol 61:1110–1117

    Article  CAS  PubMed  Google Scholar 

  • Maximov S, Ott V, Belkoura L, Kämer R (2014) Stimulus analysis of BetP activation under in vivo conditions. Biochim Biophys Acta 1838:1288–1295

    Article  CAS  PubMed  Google Scholar 

  • Mileykovskaya E, Dowhan W (2000) Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange. J Bacteriol 182:1172–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mileykovskaya E, Dowhan W, Birke RL, Zheng D, Lutterodt L, Haines TH (2001) Cardiolipin binds nonyl acridine orange by aggregating the dye at exposed hydrophobic domains on bilayer surfaces. FEBS Lett 507:187–190

    Article  CAS  PubMed  Google Scholar 

  • Mukhopadhyay R, Huang KC, Wingreen NS (2008) Lipid localization in bacterial cells through curvature-mediated microphase separation. Biophys J 95:1034–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishibori A, Kusaka J, Hara H, Umeda M, Matsumoto K (2005) Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 187:2163–2174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Norman C, Liu ZW, Rigby P, Raso A, Petrov Y, Martinac B (2005) Visualisation of the mechanosensitive channel of large conductance in bacteria using confocal microscopy. Eur Biophys J 34:396–402

    Article  PubMed  Google Scholar 

  • Oliver PM, Crooks JA, Leidl M, Yoon EJ, Saghatelian A, Weibel DB (2014) Localization of anionic phospholipids in Escherichia coli cells. J Bacteriol 196:3386–3398

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Olofsson G, Sparr E (2013) Ionization constants pKa of cardiolipin. PLoS One 8:e73040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parkin J, Chavent M, Khalid S (2015) Molecular simulations of Gram-negative bacterial membranes: a vignette of some recent successes. Biophys J 109:461–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pliotas C, Dahl ACE, Rasmussen T, Mahendran KR, Smith TK, Marius P, Gault J, Banda T, Rasmussen A, Miller S et al (2015) The role of lipids in mechanosensation. Nat Struct Mol Biol 22:991–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poolman B, Spitzer JJ, Wood JM (2004) Bacterial Osmosensing: roles of membrane structure and electrostatics in lipid-protein and protein-protein interactions. Biochim Biophys Acta 1666:88–104

    Article  CAS  PubMed  Google Scholar 

  • Quinn PJ (2012) Lipid–lipid interactions in bilayer membranes: married couples and casual liaisons. Prog Lipid Res 51:179–198

    Article  CAS  PubMed  Google Scholar 

  • Ramamurthi KS, Lecuyer S, Stone HA, Losick R (2009) Geometric cue for protein localization in a bacterium. Science 323:1354–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rasmussen T (2016) How do mechanosensitive channels sense membrane tension? Biochem Soc Trans 44:1019–1025

    Article  CAS  PubMed  Google Scholar 

  • Renner LD, Weibel DB (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci U S A 108:6264–6269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roggiani M, Goulian M (2015) Chromosome-membrane interactions in bacteria. Annu Rev Genet 49:115–129

    Article  CAS  PubMed  Google Scholar 

  • Romantsov T, Helbig S, Culham DE, Gill C, Stalker L, Wood JM (2007) Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli. Mol Microbiol 64:1455–1465

    Article  CAS  PubMed  Google Scholar 

  • Romantsov T, Stalker L, Culham DE, Wood JM (2008) Cardiolipin controls the osmotic stress response and the subcellular location of transporter ProP in Escherichia coli. J Biol Chem 283:12314–12323

    Article  CAS  PubMed  Google Scholar 

  • Romantsov T, Battle AR, Hendel JM, Martinac B, Wood JM (2009a) Protein localization in Escherichia coli cells: comparison of cytoplasmic membrane proteins ProP, LacY, ProW, AqpZ, MscS, and MscL. J Bacteriol 192:912–924

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Romantsov T, Guan Z, Wood JM (2009b) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta 1788:2092–2100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sáenz JP, Sezgin E, Schwille P, Simons K (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci U S A 109:14236–14240

    Article  PubMed  PubMed Central  Google Scholar 

  • Sevin DC, Sauer U (2014) Ubiquinone accumulation improves osmotic-stress tolerance in Escherichia coli. Nat Chem Biol 10:266–272

    Article  CAS  PubMed  Google Scholar 

  • Shaner NC, Steinbach PA, Tsien RY (2005) A guide to choosing fluorescent proteins. Nat Methods 2:905–909

    Article  CAS  PubMed  Google Scholar 

  • Shapiro L, McAdams HH, Losick R (2009) Why and how bacteria localize proteins. Science 326:1225–1228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strahl H, Burmann F, Hamoen LW (2014) The actin homologue MreB organizes the bacterial cell membrane. Nat Commun 5:3442

    Article  PubMed  CAS  Google Scholar 

  • Treuner-Lange A, Sogaard-Andersen L (2014) Regulation of cell polarity in bacteria. J Cell Biol 206:7–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsatskis Y, Khambati J, Dobson M, Bogdanov M, Dowhan W, Wood JM (2005) The osmotic activation of transporter ProP is tuned by both its C-terminal coiled-coil and osmotically induced changes in phospholipid composition. J Biol Chem 280:41387–41394

    Article  CAS  PubMed  Google Scholar 

  • Tsuzuki M, Moskvin OV, Kuribayashi M, Sato K, Retamal S, Abo M (2011) Salt stress-induced changes in the transcriptome, compatible solutes, and membrane lipids in the facultatively phototrophic bacterium Rhodobacter sphaeroides. Appl Environ Microbiol 77:7551–7559.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanounou S, Pines D, Pines E, Parola AH, Fishov I (2002) Coexistence of domains with distinct order and polarity in fluid bacterial membranes. Photochem Photobiol 76:1–11

    Article  CAS  PubMed  Google Scholar 

  • Vanounou S, Parola AH, Fishov I (2003) Phosphatidylethanolamine and phosphatidylglycerol are segregated into different domains in bacterial membrane. A study with pyrene-labelled phospholipids. Mol Microbiol 49:1067–1079

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Black SS, Edwards MD, Miller S, Bartlett W, Dong C, Naismith J, Booth IR (2008) The structure of an open form of an E. coli mechanosensitive channel reveals the molecular basis of gating. Science 321:1179–1183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolters JC, Berntsson RP, Gul N, Karasawa A, Thunnissen AM, Slotboom DJ, Poolman B (2010) Ligand binding and crystal structures of the substrate-binding domain of the ABC transporter OpuA. PLoS One 5:e10361

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wood JM (1999) Osmosensing by bacteria: signals and membrane-based sensors. Microbiol Mol Biol Rev 63:230–262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wood JM (2007) Bacterial osmosensing transporters. Methods Enzymol 428:77–107

    Article  CAS  PubMed  Google Scholar 

  • Wood JM (2011) Bacterial osmoregulation: a paradigm for the study of cellular homeostasis. Annu Rev Microbiol 65:215–238

    Article  CAS  PubMed  Google Scholar 

  • Wood JM (2015) Bacterial responses to osmotic challenges. J Gen Physiol 145:381–388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu EL, Cheng X, Jo S, Rui H, Song KC, Davila-Contreras EM, Qi YF, Lee JM, Monje-Galvan V, Venable RM et al (2014) CHARMM-GUI membrane builder toward realistic biological membrane simulations. J Comput Chem 35:1997–2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeagle PL (2011) The structure of biological membranes, 3rd edn. CRC Press, Boca Raton

    Book  Google Scholar 

  • Zaritsky A, Woldringh C, Fishov I, Vischer NO, Einav M (1999) Varying division planes of secondary constrictions in spheroidal Escherichia coli cells. Microbiology 145:1015–1022

    Article  CAS  PubMed  Google Scholar 

  • Zhang XC, Liu Z, Li J (2016) From membrane tension to channel gating: a principal energy transfer mechanism for mechanosensitive channels. Protein Sci 25:1954–1964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong D, Blount P (2014) Electrostatics at the membrane define MscL channel mechanosensitivity and kinetics. FASEB J 28:5234–5241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zoetewey DL, Tripet BP, Kutateladze TG, Overduin MJ, Wood JM, Hodges RS (2003) Solution structure of the C-terminal antiparallel coiled-coil domain from Escherichia coli osmosensor ProP. J Mol Biol 334:1063–1076

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

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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Romantsov, T., Wood, J.M. (2019). Contributions of Membrane Lipids to Bacterial Cell Homeostasis upon Osmotic Challenge. In: Geiger, O. (eds) Biogenesis of Fatty Acids, Lipids and Membranes. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50430-8_58

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