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Organization and function of anionic phospholipids in bacteria

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Abstract

In addition to playing a central role as a permeability barrier for controlling the diffusion of molecules and ions in and out of bacterial cells, phospholipid (PL) membranes regulate the spatial and temporal position and function of membrane proteins that play an essential role in a variety of cellular functions. Based on the very large number of membrane-associated proteins encoded in genomes, an understanding of the role of PLs may be central to understanding bacterial cell biology. This area of microbiology has received considerable attention over the past two decades, and the local enrichment of anionic PLs has emerged as a candidate mechanism for biomolecular organization in bacterial cells. In this review, we summarize the current understanding of anionic PLs in bacteria, including their biosynthesis, subcellular localization, and physiological relevance, discuss evidence and mechanisms for enriching anionic PLs in membranes, and conclude with an assessment of future directions for this area of bacterial biochemistry, biophysics, and cell biology.

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References

  • Alley SH, Ces O, Barahona M, Templer RH (2008) X-ray diffraction measurement of the monolayer spontaneous curvature of dioleoylphosphatidylglycerol. Chem Phys Lipid 154(1):64–67

    Article  CAS  Google Scholar 

  • Arechaga I (2013) Membrane invaginations in bacteria and mitochondria: common features and evolutionary scenarios. J Mol Microbiol Biotechnol 23(1–2):13–23

    Article  CAS  PubMed  Google Scholar 

  • Arias-Cartin R, Grimaldi S, Pommier J, Lanciano P, Schaefer C, Arnoux P, Giordano G, Guigliarelli B, Magalon A (2011) Cardiolipin-based respiratory complex activation in bacteria. Proc Natl Acad Sci U S A 108(19):7781–7786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arias-Cartin R, Grimaldi S, Arnoux P, Guigliarelli B, Magalon A (2012) Cardiolipin binding in bacterial respiratory complexes: structural and functional implications. Biochim Biophys Acta 1817(10):1937–1949

    Article  CAS  PubMed  Google Scholar 

  • Barak I, Muchova K (2013) The role of lipid domains in bacterial cell processes. Int J Mol Sci 14(2):4050–4065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barak I, Muchova K, Wilkinson AJ, O’Toole PJ, Pavlendova N (2008) Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 68(5):1315–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ben-Yehuda S, Losick R (2002) Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109(2):257–266

    Article  CAS  PubMed  Google Scholar 

  • Bernal P, Munoz-Rojas J, Hurtado A, Ramos JL, Segura A (2007) A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality. Environ Microbiol 9(5):1135–1145

    Article  CAS  PubMed  Google Scholar 

  • Binenbaum Z, Parola AH, Zaritsky A, Fishov I (1999) Transcription- and translation-dependent changes in membrane dynamics in bacteria: testing the transertion model for domain formation. Mol Microbiol 32(6):1173–1182

    Article  CAS  PubMed  Google Scholar 

  • Boeneman K, Fossum S, Yang Y, Fingland N, Skarstad K, Crooke E (2009) Escherichia coli DnaA forms helical structures along the longitudinal cell axis distinct from MreB filaments. Mol Microbiol 72(3):645–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bramkamp M, Emmins R, Weston L, Donovan C, Daniel RA, Errington J (2008) A novel component of the division-site selection system of Bacillus subtilis and a new mode of action for the division inhibitor MinCD. Mol Microbiol 70(6):1556–1569

    Article  CAS  PubMed  Google Scholar 

  • Camberg JL, Johnson TL, Patrick M, Abendroth J, Hol WG, Sandkvist M (2007) Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids. EMBO J 26(1):19–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campo N, Tjalsma H, Buist G, Stepniak D, Meijer M, Veenhuis M, Westermann M, Muller JP, Bron S, Kok J, Kuipers OP, Jongbloed JD (2004) Subcellular sites for bacterial protein export. Mol Microbiol 53(6):1583–1599

    Article  CAS  PubMed  Google Scholar 

  • Castuma CE, Crooke E, Kornberg A (1993) Fluid membranes with acidic domains activate DnaA, the initiator protein of replication in Escherichia coli. J Biol Chem 268(33):24665–24668

    CAS  PubMed  Google Scholar 

  • Catucci L, Depalo N, Lattanzio VM, Agostiano A, Corcelli A (2004) Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochemistry 43(47):15066–15072

    Article  CAS  PubMed  Google Scholar 

  • Cayley DS, Guttman HJ, Record MT Jr (2000) Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys J 78(4):1748–1764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chory J, Donohue TJ, Varga AR, Staehelin LA, Kaplan S (1984) Induction of the photosynthetic membranes of Rhodopseudomonas sphaeroides: biochemical and morphological studies. J Bacteriol 159(2):540–554

    CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen H, Garton NJ, Horobin RW, Minnikin DE, Barer MR (1999) Lipid domains of mycobacteria studied with fluorescent molecular probes. Mole Microbiol 31(5):1561–1572

    Article  CAS  Google Scholar 

  • Conrad RS, Gilleland HE Jr (1981) Lipid alterations in cell envelopes of polymyxin-resistant Pseudomonas aeruginosa isolates. J Bacteriol 148(2):487–497

    CAS  PubMed  PubMed Central  Google Scholar 

  • Contreras I, Shapiro L, Henry S (1978) Membrane phospholipid composition of Caulobacter crescentus. J Bacteriol 135(3):1130–1136

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crooke E, Castuma CE, Kornberg A (1992) The chromosome origin of Escherichia coli stabilizes DnaA protein during rejuvenation by phospholipids. J Biol Chem 267(24):16779–16782

    CAS  PubMed  Google Scholar 

  • Dalebroux ZD, Matamouros S, Whittington D, Bishop RE, Miller SI (2014) PhoPQ regulates acidic glycerophospholipid content of the Salmonella Typhimurium outer membrane. Proc Natl Acad Sci U S A 111(5):1963–1968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dalebroux ZD, Edrozo MB, Pfuetzner RA, Ressl S, Kulasekara BR, Blanc MP, Miller SI (2015) Delivery of cardiolipins to the Salmonella outer membrane is necessary for survival within host tissues and virulence. Cell Host Microbe 17(4):441–451

    Article  CAS  PubMed  Google Scholar 

  • Dancey GF, Shapiro BM (1977) Specific phospholipid requirement for activity of the purified respiratory chain NADH dehydrogenase of Escherichia coli. Biochim Biophys Acta 487(2):368–377

    Article  CAS  PubMed  Google Scholar 

  • de Vrije T, de Swart RL, Dowhan W, Tommassen J, de Kruijff B (1988) Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature 334(6178):173–175

    Article  PubMed  Google Scholar 

  • Domenech O, Sanz F, Montero MT, Hernandez-Borrell J (2006) Thermodynamic and structural study of the main phospholipid components comprising the mitochondrial inner membrane. Biochim Biophys Acta 1758(2):213–221

    Article  CAS  PubMed  Google Scholar 

  • Domenech O, Morros A, Cabanas ME, Montero MT, Hernandez-Borrell J (2007) Thermal response of domains in cardiolipin content bilayers. Ultramicroscopy 107(10–11):943–947

    Article  CAS  PubMed  Google Scholar 

  • Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232

    Article  CAS  PubMed  Google Scholar 

  • Drew DA, Osborn MJ, Rothfield LI (2005) A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement. Proc Natl Acad Sci U S A 102(17):6114–6118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards DH, Errington J (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24(5):905–915

    Article  CAS  PubMed  Google Scholar 

  • Epand RF, Tokarska-Schlattner M, Schlattner U, Wallimann T, Epand RM (2007) Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J Mol Biol 365(4):968–980

    Article  CAS  PubMed  Google Scholar 

  • Esfahani M, Rudkin BB, Cutler CJ, Waldron PE (1977) Lipid-protein interactions in membranes: interaction of phospholipids with respiratory enzymes of Escherichia coli membrane. J Biol Chem 252(10):3194–3198

    CAS  PubMed  Google Scholar 

  • Fingland N, Flatten I, Downey CD, Fossum-Raunehaug S, Skarstad K, Crooke E (2012) Depletion of acidic phospholipids influences chromosomal replication in Escherichia coli. Microbiol Open 1(4):450–466

    Article  CAS  Google Scholar 

  • Fishov I, Woldringh CL (1999) Visualization of membrane domains in Escherichia coli. Mol Microbiol 32(6):1166–1172

    Article  CAS  PubMed  Google Scholar 

  • Foss MH, Eun YJ, Weibel DB (2011) Chemical-biological studies of subcellular organization in bacteria. Biochemistry 50(36):7719–7734

    Article  CAS  PubMed  Google Scholar 

  • Gmeiner J, Martin HH (1976) Phospholipid and lipopolysaccharide in Proteus mirabilis and its stable protoplast L-form. Difference in content and fatty acid composition. Eur J Biochem 67(2):487–494

    Article  CAS  PubMed  Google Scholar 

  • Gold VA, Robson A, Bao H, Romantsov T, Duong F, Collinson I (2010) The action of cardiolipin on the bacterial translocon. Proc Natl Acad Sci U S A 107(22):10044–10049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamai C, Yang T, Kataoka S, Cremer PS, Musser SM (2006) Effect of average phospholipid curvature on supported bilayer formation on glass by vesicle fusion. Biophys J 90(4):1241–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiraoka S, Matsuzaki H, Shibuya I (1993) Active increase in cardiolipin synthesis in the stationary growth phase and its physiological significance in Escherichia coli. FEBS Lett 336(2):221–224

    Article  CAS  PubMed  Google Scholar 

  • Hsieh CW, Lin TY, Lai HM, Lin CC, Hsieh TS, Shih YL (2010) Direct MinE-membrane interaction contributes to the proper localization of MinDE in E. coli. Mol Microbiol 75(2):499–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang KC, Mukhopadhyay R, Wingreen NS (2006) A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput Biol 2(11):e151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jormakka M, Tornroth S, Byrne B, Iwata S (2002) Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295(5561):1863–1868

    Article  PubMed  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(1):181–197

    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(10):877–882

    Article  CAS  PubMed  Google Scholar 

  • Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H, Matsumoto K (2004) Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186(5):1475–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennell D, Riezman H (1977) Transcription and translation initiation frequencies of the Escherichia coli lac operon. J Mol Biol 114(1):1–21

    Article  CAS  PubMed  Google Scholar 

  • Kitchen JL, Li Z, Crooke E (1999) Electrostatic interactions during acidic phospholipid reactivation of DnaA protein, the Escherichia coli initiator of chromosomal replication. Biochemistry 38(19):6213–6221

    Article  CAS  PubMed  Google Scholar 

  • Koch AL, Pinette MF (1987) Nephelometric determination of turgor pressure in growing Gram-negative bacteria. J Bacteriol 169(8):3654–3663

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koppelman CM, Den Blaauwen T, Duursma MC, Heeren RM, Nanninga N (2001) Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 183(20):6144–6147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprivnjak T, Zhang D, Ernst CM, Peschel A, Nauseef WM, Weiss JP (2011) Characterization of Staphylococcus aureus cardiolipin synthases 1 and 2 and their contribution to accumulation of cardiolipin in stationary phase and within phagocytes. J Bacteriol 193(16):4134–4142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn S, Slavetinsky CJ, Peschel A (2015) Synthesis and function of phospholipids in Staphylococcus aureus. Int J Med Microbiol 305(2):196–202

    Article  CAS  PubMed  Google Scholar 

  • Laage S, Tao Y, McDermott AE (2015) Cardiolipin interaction with subunit c of ATP synthase: solid-state NMR characterization. Biochim Biophys Acta 1848(1 Pt B):260–265

    Article  CAS  PubMed  Google Scholar 

  • Lenarcic R, Halbedel S, Visser L, Shaw M, Wu LJ, Errington J, Marenduzzo D, Hamoen LW (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28(15):2272–2282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leung CW, Hong Y, Hanske J, Zhao E, Chen S, Pletneva EV, Tang BZ (2014) Superior fluorescent probe for detection of cardiolipin. Anal Chem 86(2):1263–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lill R, Dowhan W, Wickner W (1990) The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60(2):271–280

    Article  CAS  PubMed  Google Scholar 

  • Lin TY, Santos TM, Kontur WS, Donohue TJ, Weibel DB (2015) A cardiolipin-deficient mutant of Rhodobacter sphaeroides has an altered cell shape and is impaired in biofilm formation. J Bacteriol 197(21):3446–3455

    Article  CAS  PubMed  Google Scholar 

  • Linde K, Grobner G, Rilfors L (2004) Lipid dependence and activity control of phosphatidylserine synthase from Escherichia coli. FEBS Lett 575(1–3):77–80

    Article  CAS  PubMed  Google Scholar 

  • Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46–50

    Article  CAS  PubMed  Google Scholar 

  • Lopez CS, Alice AF, Heras H, Rivas EA, Sanchez-Rivas C (2006) Role of anionic phospholipids in the adaptation of Bacillus subtilis to high salinity. Microbiology 152(Pt 3):605–616

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto K (2001) Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol Microbiol 39(6):1427–1433

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto K, Kusaka J, Nishibori A, Hara H (2006) Lipid domains in bacterial membranes. Mol Microbiol 61(5):1110–1117

    Article  CAS  PubMed  Google Scholar 

  • McAuley KE, Fyfe PK, Ridge JP, Isaacs NW, Cogdell RJ, Jones MR (1999) Structural details of an interaction between cardiolipin and an integral membrane protein. Proc Natl Acad Sci U S A 96(26):14706–14711

    Article  CAS  PubMed  PubMed Central  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(4):1172–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mileykovskaya E, Dowhan W (2005) Role of membrane lipids in bacterial division-site selection. Curr Opin Microbiol 8(2):135–142

    Article  CAS  PubMed  Google Scholar 

  • Mileykovskaya E, Dowhan W (2009) Cardiolipin membrane domains in prokaryotes and eukaryotes. Biochim Biophys Acta 1788(10):2084–2091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mileykovskaya E, Fishov I, Fu X, Corbin BD, Margolin W, Dowhan W (2003) Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 278(25):22193–22198

    Article  CAS  PubMed  Google Scholar 

  • Mileykovskaya E, Ryan AC, Mo X, Lin CC, Khalaf KI, Dowhan W, Garrett TA (2009) Phosphatidic acid and N-acylphosphatidylethanolamine form membrane domains in Escherichia coli mutant lacking cardiolipin and phosphatidylglycerol. J Biol Chem 284(5):2990–3000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muchova K, Wilkinson AJ, Barak I (2011) Changes of lipid domains in Bacillus subtilis cells with disrupted cell wall peptidoglycan. FEMS Microbiol Lett 325(1):92–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay R, Huang KC, Wingreen NS (2008) Lipid localization in bacterial cells through curvature-mediated microphase separation. Biophys J 95(3):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(6):2163–2174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishijima S, Asami Y, Uetake N, Yamagoe S, Ohta A, Shibuya I (1988) Disruption of the Escherichia coli cls gene responsible for cardiolipin synthesis. J Bacteriol 170(2):775–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Norris V (1995) Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol Microbiol 16(6):1051–1057

    Article  CAS  PubMed  Google Scholar 

  • Ohniwa RL, Kitabayashi K, Morikawa K (2013) Alternative cardiolipin synthase Cls1 compensates for stalled Cls2 function in Staphylococcus aureus under conditions of acute acid stress. FEMS Microbiol Lett 338(2):141–146

    Article  CAS  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(19):3386–3398

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petit JM, Maftah A, Ratinaud MH, Julien R (1992) 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 209(1):267–273

    Article  CAS  PubMed  Google Scholar 

  • Petit JM, Huet O, Gallet PF, Maftah A, Ratinaud MH, Julien R (1994) Direct analysis and significance of cardiolipin transverse distribution in mitochondrial inner membranes. Eur J Biochem 220(3):871–879

    Article  CAS  PubMed  Google Scholar 

  • Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459(7245):379–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polyansky AA, Volynsky RRPE, Sbalzarini IF, Marrink SJ, Efremov RG (2010) Antimicrobial peptides induce growth of phosphatidylglycerol domains in a model bacterial membrane. J Phys Chem Lett 1(20):3108–3111

    Article  CAS  Google Scholar 

  • Powell GL, Hui SW (1996) Tetraoleoylpyrophosphatidic acid: a four acyl-chain lipid which forms a hexagonal II phase with high curvature. Biophys J 70(3):1402–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ragolia L, Tropp BE (1994) The effects of phosphoglycerides on Escherichia coli cardiolipin synthase. Biochim Biophys Acta 1214(3):323–332

    Article  PubMed  Google Scholar 

  • Rajendram M, Zhang L, Reynolds BJ, Auer GK, Tuson HH, Ngo KV, Cox MM, Yethiraj A, Cui Q, Weibel DB (2015) Anionic phospholipids stabilize RecA filament bundles in Escherichia coli. Mol Cell 60(3):374–384

    Article  CAS  PubMed  Google Scholar 

  • Ramamurthi KS, Losick R (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci U S A 106(32):13541–13545

    Article  CAS  PubMed  PubMed Central  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(15):6264–6269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renner LD, Weibel DB (2012) MinD and MinE interact with anionic phospholipids and regulate division plane formation in Escherichia coli. J Biol Chem 287(46):38835–38844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renner LD, Eswaramoorthy P, Ramamurthi KS, Weibel DB (2013) Studying biomolecule localization by engineering bacterial cell wall curvature. PLoS One 8(12):e84143

    Article  PubMed  PubMed Central  CAS  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(6):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(18):12314–12323

    Article  CAS  PubMed  Google Scholar 

  • Romantsov T, Guan Z, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta 1788(10):2092–2100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosch JW, Hsu FF, Caparon MG (2007) Anionic lipids enriched at the ExPortal of Streptococcus pyogenes. J Bacteriol 189(3):801–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salamon Z, Lindblom G, Rilfors L, Linde K, Tollin G (2000) Interaction of phosphatidylserine synthase from E. coli with lipid bilayers: coupled plasmon-waveguide resonance spectroscopy studies. Biophys J 78(3):1400–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandoval-Calderon M, Geiger O, Guan Z, Barona-Gomez F, Sohlenkamp C (2009) A eukaryote-like cardiolipin synthase is present in Streptomyces coelicolor and in most actinobacteria. J Biol Chem 284(26):17383–17390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena R, Fingland N, Patil D, Sharma AK, Crooke E (2013) Crosstalk between DnaA protein, the initiator of Escherichia coli chromosomal replication, and acidic phospholipids present in bacterial membranes. Int J Mol Sci 14(4):8517–8537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sekimizu K, Kornberg A (1988) Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J Biol Chem 263(15):7131–7135

    CAS  PubMed  Google Scholar 

  • Sennato S, Bordi F, Cametti C, Coluzza C, Desideri A, Rufini S (2005) Evidence of domain formation in cardiolipin-glycerophospholipid mixed monolayers. A thermodynamic and AFM study. J Phys Chem B 109(33):15950–15957

    Article  CAS  PubMed  Google Scholar 

  • Shibuya I, Miyazaki C, Ohta A (1985) Alteration of phospholipid composition by combined defects in phosphatidylserine and cardiolipin synthases and physiological consequences in Escherichia coli. J Bacteriol 161(3):1086–1092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shih YL, Le T, Rothfield L (2003) Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc Natl Acad Sci U S A 100(13):7865–7870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shih YL, Huang KF, Lai HM, Liao JH, Lee CS, Chang CM, Mak HM, Hsieh CW, Lin CC (2011) The N-terminal amphipathic helix of the topological specificity factor MinE is associated with shaping membrane curvature. PLoS One 6(6):e21425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2(5):a000414

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175(4023):720–731

    Article  CAS  PubMed  Google Scholar 

  • Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 40(1):133–159

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan BK, Bogdanov M, Zhao J, Dowhan W, Raetz CR, Guan Z (2012) Discovery of a cardiolipin synthase utilizing phosphatidylethanolamine and phosphatidylglycerol as substrates. Proc Natl Acad Sci U S A 109(41):16504–16509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Anraku Y, Futai M (1976) Escherichia coli membrane D-lactate dehydrogenase. Isolation of the enzyme in aggregated from and its activation by Triton X-100 and phospholipids. J Biochem 80(4):821–830

    CAS  PubMed  Google Scholar 

  • Tomsie N, Babnik B, Lombardo D, Mavcic B, Kanduser M, Iglic A, Kralj-Iglic V (2005) Shape and size of giant unilamellar phospholipid vesicles containing cardiolipin. J Chem Inf Model 45(6):1676–1679

    Article  CAS  PubMed  Google Scholar 

  • Trombe MC, Laneelle MA, Laneelle G (1979) Lipid composition of aminopterin-resistant and sensitive strains of Streptococcus pneumoniae. Effect of aminopterin inhibition. Biochim Biophys Acta 574(2):290–300

    Article  CAS  PubMed  Google Scholar 

  • Tsai M, Ohniwa RL, Kato Y, Takeshita SL, Ohta T, Saito S, Hayashi H, Morikawa K (2011) Staphylococcus aureus requires cardiolipin for survival under conditions of high salinity. BMC Microbiol 11:13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unsay JD, Cosentino K, Subburaj Y, Garcia-Saez AJ (2013) Cardiolipin effects on membrane structure and dynamics. Langmuir 29(51):15878–15887

    Article  CAS  PubMed  Google Scholar 

  • Ursell TS, Nguyen J, Monds RD, Colavin A, Billings G, Ouzounov N, Gitai Z, Shaevitz JW, Huang KC (2014) Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc Natl Acad Sci U S A 111(11):E1025–E1034

    Article  CAS  PubMed  PubMed Central  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(4):1067–1079

    Article  CAS  PubMed  Google Scholar 

  • Vecchiarelli AG, Li M, Mizuuchi M, Mizuuchi K (2014) Differential affinities of MinD and MinE to anionic phospholipid influence Min patterning dynamics in vitro. Mol Microbiol 93(3):453–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber TA, Koob S, Heide H, Wittig I, Head B, van der Bliek A, Brandt U, Mittelbronn M, Reichert AS (2013) APOOL is a cardiolipin-binding constituent of the Mitofilin/MINOS protein complex determining cristae morphology in mammalian mitochondria. PLoS One 8(5):e63683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yankovskaya V, Horsefield R, Tornroth S, Luna-Chavez C, Miyoshi H, Leger C, Byrne B, Cecchini G, Iwata S (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299(5607):700–704

    Article  CAS  PubMed  Google Scholar 

  • Yao X, Jericho M, Pink D, Beveridge T (1999) Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J Bacteriol 181(22):6865–6875

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yung BY, Kornberg A (1988) Membrane attachment activates dnaA protein, the initiation protein of chromosome replication in Escherichia coli. Proc Natl Acad Sci U S A 85(19):7202–7205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6(3):222–233

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Tamot B, Hiser C, Reid GE, Benning C, Ferguson-Miller S (2011) Cardiolipin deficiency in Rhodobacter sphaeroides alters the lipid profile of membranes and of crystallized cytochrome oxidase, but structure and function are maintained. Biochemistry 50(19):3879–3890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zieske K, Schwille P (2014) Reconstitution of self-organizing protein gradients as spatial cues in cell-free systems. eLife 3:e03949

    Article  PubMed Central  CAS  Google Scholar 

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Acknowledgments

T.-Y. Lin acknowledges a Dr. James Chieh-Hsia Mao Wisconsin Distinguished Graduate Fellowship from the Department of Biochemistry, University of Wisconsin-Madison. Research in this area of our lab is supported by the National Science Foundation (under award DMR-1121288), the National Institutes of Health (1DP2OD008735), and the United States Department of Agriculture (WIS01594).

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Authors and Affiliations

  1. Department of Biochemistry, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Ti-Yu Lin & Douglas B. Weibel

  2. Department of Biomedical Engineering, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Douglas B. Weibel

  3. Department of Chemistry, University of Wisconsin-Madison, Madison, WI, 53706, USA

    Douglas B. Weibel

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  1. Ti-Yu Lin
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  2. Douglas B. Weibel
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Correspondence to Douglas B. Weibel.

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Ti-Yu Lin declares that he has no conflict of interest. Douglas B. Weibel declares that he has no conflict of interest.

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Lin, TY., Weibel, D.B. Organization and function of anionic phospholipids in bacteria. Appl Microbiol Biotechnol 100, 4255–4267 (2016). https://doi.org/10.1007/s00253-016-7468-x

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  • DOI: https://doi.org/10.1007/s00253-016-7468-x

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