Applied Microbiology and Biotechnology

, Volume 100, Issue 10, pp 4255–4267 | Cite as

Organization and function of anionic phospholipids in bacteria

  • Ti-Yu Lin
  • Douglas B. WeibelEmail author


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.


Anionic phospholipids Cardiolipin Subcellular localization Bacteria Cell Membrane curvature 



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).

Compliance with ethical standards

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

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


  1. 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):64–67CrossRefGoogle Scholar
  2. Arechaga I (2013) Membrane invaginations in bacteria and mitochondria: common features and evolutionary scenarios. J Mol Microbiol Biotechnol 23(1–2):13–23PubMedCrossRefGoogle Scholar
  3. 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):7781–7786PubMedPubMedCentralCrossRefGoogle Scholar
  4. 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):1937–1949PubMedCrossRefGoogle Scholar
  5. Barak I, Muchova K (2013) The role of lipid domains in bacterial cell processes. Int J Mol Sci 14(2):4050–4065PubMedPubMedCentralCrossRefGoogle Scholar
  6. 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):1315–1327PubMedPubMedCentralCrossRefGoogle Scholar
  7. 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):257–266PubMedCrossRefGoogle Scholar
  8. 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):1135–1145PubMedCrossRefGoogle Scholar
  9. 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):1173–1182PubMedCrossRefGoogle Scholar
  10. 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):645–657PubMedPubMedCentralCrossRefGoogle Scholar
  11. 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):1556–1569PubMedCrossRefGoogle Scholar
  12. 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):19–27PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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):1583–1599PubMedCrossRefGoogle Scholar
  14. 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):24665–24668PubMedGoogle Scholar
  15. Catucci L, Depalo N, Lattanzio VM, Agostiano A, Corcelli A (2004) Neosynthesis of cardiolipin in Rhodobacter sphaeroides under osmotic stress. Biochemistry 43(47):15066–15072PubMedCrossRefGoogle Scholar
  16. 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):1748–1764PubMedPubMedCentralCrossRefGoogle Scholar
  17. 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):540–554PubMedPubMedCentralGoogle Scholar
  18. Christensen H, Garton NJ, Horobin RW, Minnikin DE, Barer MR (1999) Lipid domains of mycobacteria studied with fluorescent molecular probes. Mole Microbiol 31(5):1561–1572CrossRefGoogle Scholar
  19. Conrad RS, Gilleland HE Jr (1981) Lipid alterations in cell envelopes of polymyxin-resistant Pseudomonas aeruginosa isolates. J Bacteriol 148(2):487–497PubMedPubMedCentralGoogle Scholar
  20. Contreras I, Shapiro L, Henry S (1978) Membrane phospholipid composition of Caulobacter crescentus. J Bacteriol 135(3):1130–1136PubMedPubMedCentralGoogle Scholar
  21. 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):16779–16782PubMedGoogle Scholar
  22. 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):1963–1968PubMedPubMedCentralCrossRefGoogle Scholar
  23. 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):441–451PubMedCrossRefGoogle Scholar
  24. 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):368–377PubMedCrossRefGoogle Scholar
  25. 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):173–175PubMedCrossRefGoogle Scholar
  26. 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):213–221PubMedCrossRefGoogle Scholar
  27. Domenech O, Morros A, Cabanas ME, Montero MT, Hernandez-Borrell J (2007) Thermal response of domains in cardiolipin content bilayers. Ultramicroscopy 107(10–11):943–947PubMedCrossRefGoogle Scholar
  28. Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232PubMedCrossRefGoogle Scholar
  29. 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):6114–6118PubMedPubMedCentralCrossRefGoogle Scholar
  30. 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):905–915PubMedCrossRefGoogle Scholar
  31. 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):968–980PubMedCrossRefGoogle Scholar
  32. 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):3194–3198PubMedGoogle Scholar
  33. 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):450–466CrossRefGoogle Scholar
  34. Fishov I, Woldringh CL (1999) Visualization of membrane domains in Escherichia coli. Mol Microbiol 32(6):1166–1172PubMedCrossRefGoogle Scholar
  35. Foss MH, Eun YJ, Weibel DB (2011) Chemical-biological studies of subcellular organization in bacteria. Biochemistry 50(36):7719–7734PubMedCrossRefGoogle Scholar
  36. 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):487–494PubMedCrossRefGoogle Scholar
  37. 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):10044–10049PubMedPubMedCentralCrossRefGoogle Scholar
  38. 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):1241–1248PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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):221–224PubMedCrossRefGoogle Scholar
  40. 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):499–512PubMedPubMedCentralCrossRefGoogle Scholar
  41. Huang KC, Mukhopadhyay R, Wingreen NS (2006) A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput Biol 2(11):e151PubMedPubMedCentralCrossRefGoogle Scholar
  42. Jormakka M, Tornroth S, Byrne B, Iwata S (2002) Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295(5561):1863–1868PubMedCrossRefGoogle Scholar
  43. 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):181–197PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kates M, Syz JY, Gosser D, Haines TH (1993) pH-dissociation characteristics of cardiolipin and its 2’-deoxy analogue. Lipids 28(10):877–882PubMedCrossRefGoogle Scholar
  45. Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H, Matsumoto K (2004) Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186(5):1475–1483PubMedPubMedCentralCrossRefGoogle Scholar
  46. Kennell D, Riezman H (1977) Transcription and translation initiation frequencies of the Escherichia coli lac operon. J Mol Biol 114(1):1–21PubMedCrossRefGoogle Scholar
  47. 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):6213–6221PubMedCrossRefGoogle Scholar
  48. Koch AL, Pinette MF (1987) Nephelometric determination of turgor pressure in growing Gram-negative bacteria. J Bacteriol 169(8):3654–3663PubMedPubMedCentralGoogle Scholar
  49. Koppelman CM, Den Blaauwen T, Duursma MC, Heeren RM, Nanninga N (2001) Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 183(20):6144–6147PubMedPubMedCentralCrossRefGoogle Scholar
  50. 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):4134–4142PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kuhn S, Slavetinsky CJ, Peschel A (2015) Synthesis and function of phospholipids in Staphylococcus aureus. Int J Med Microbiol 305(2):196–202PubMedCrossRefGoogle Scholar
  52. 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):260–265PubMedCrossRefGoogle Scholar
  53. 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):2272–2282PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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):1263–1268PubMedPubMedCentralCrossRefGoogle Scholar
  55. 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):271–280PubMedCrossRefGoogle Scholar
  56. 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):3446–3455PubMedCrossRefGoogle Scholar
  57. Linde K, Grobner G, Rilfors L (2004) Lipid dependence and activity control of phosphatidylserine synthase from Escherichia coli. FEBS Lett 575(1–3):77–80PubMedCrossRefGoogle Scholar
  58. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327(5961):46–50PubMedCrossRefGoogle Scholar
  59. 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):605–616PubMedCrossRefGoogle Scholar
  60. Matsumoto K (2001) Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol Microbiol 39(6):1427–1433PubMedCrossRefGoogle Scholar
  61. Matsumoto K, Kusaka J, Nishibori A, Hara H (2006) Lipid domains in bacterial membranes. Mol Microbiol 61(5):1110–1117PubMedCrossRefGoogle Scholar
  62. 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):14706–14711PubMedPubMedCentralCrossRefGoogle Scholar
  63. 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):1172–1175PubMedPubMedCentralCrossRefGoogle Scholar
  64. Mileykovskaya E, Dowhan W (2005) Role of membrane lipids in bacterial division-site selection. Curr Opin Microbiol 8(2):135–142PubMedCrossRefGoogle Scholar
  65. Mileykovskaya E, Dowhan W (2009) Cardiolipin membrane domains in prokaryotes and eukaryotes. Biochim Biophys Acta 1788(10):2084–2091PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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):22193–22198PubMedCrossRefGoogle Scholar
  67. 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):2990–3000PubMedPubMedCentralCrossRefGoogle Scholar
  68. 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):92–98PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mukhopadhyay R, Huang KC, Wingreen NS (2008) Lipid localization in bacterial cells through curvature-mediated microphase separation. Biophys J 95(3):1034–1049PubMedPubMedCentralCrossRefGoogle Scholar
  70. 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):2163–2174PubMedPubMedCentralCrossRefGoogle Scholar
  71. 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):775–780PubMedPubMedCentralGoogle Scholar
  72. Norris V (1995) Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol Microbiol 16(6):1051–1057PubMedCrossRefGoogle Scholar
  73. 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):141–146PubMedCrossRefGoogle Scholar
  74. 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):3386–3398PubMedPubMedCentralCrossRefGoogle Scholar
  75. 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):267–273PubMedCrossRefGoogle Scholar
  76. 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):871–879PubMedCrossRefGoogle Scholar
  77. Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane-protein function. Nature 459(7245):379–385PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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):3108–3111CrossRefGoogle Scholar
  79. 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):1402–1406PubMedPubMedCentralCrossRefGoogle Scholar
  80. Ragolia L, Tropp BE (1994) The effects of phosphoglycerides on Escherichia coli cardiolipin synthase. Biochim Biophys Acta 1214(3):323–332PubMedCrossRefGoogle Scholar
  81. 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):374–384PubMedCrossRefGoogle Scholar
  82. 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):13541–13545PubMedPubMedCentralCrossRefGoogle Scholar
  83. 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):6264–6269PubMedPubMedCentralCrossRefGoogle Scholar
  84. 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):38835–38844PubMedPubMedCentralCrossRefGoogle Scholar
  85. Renner LD, Eswaramoorthy P, Ramamurthi KS, Weibel DB (2013) Studying biomolecule localization by engineering bacterial cell wall curvature. PLoS One 8(12):e84143PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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):1455–1465PubMedCrossRefGoogle Scholar
  87. 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):12314–12323PubMedCrossRefGoogle Scholar
  88. Romantsov T, Guan Z, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta 1788(10):2092–2100PubMedPubMedCentralCrossRefGoogle Scholar
  89. Rosch JW, Hsu FF, Caparon MG (2007) Anionic lipids enriched at the ExPortal of Streptococcus pyogenes. J Bacteriol 189(3):801–806PubMedPubMedCentralCrossRefGoogle Scholar
  90. 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):1400–1412PubMedPubMedCentralCrossRefGoogle Scholar
  91. 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):17383–17390PubMedPubMedCentralCrossRefGoogle Scholar
  92. 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):8517–8537PubMedPubMedCentralCrossRefGoogle Scholar
  93. Sekimizu K, Kornberg A (1988) Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J Biol Chem 263(15):7131–7135PubMedGoogle Scholar
  94. 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):15950–15957PubMedCrossRefGoogle Scholar
  95. 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):1086–1092PubMedPubMedCentralGoogle Scholar
  96. 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):7865–7870PubMedPubMedCentralCrossRefGoogle Scholar
  97. 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):e21425PubMedPubMedCentralCrossRefGoogle Scholar
  98. Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2(5):a000414PubMedPubMedCentralCrossRefGoogle Scholar
  99. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175(4023):720–731PubMedCrossRefGoogle Scholar
  100. Sohlenkamp C, Geiger O (2016) Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev 40(1):133–159PubMedCrossRefGoogle Scholar
  101. Strahl H, Burmann F, Hamoen LW (2014) The actin homologue MreB organizes the bacterial cell membrane. Nat Commun 5:3442PubMedPubMedCentralCrossRefGoogle Scholar
  102. 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):16504–16509PubMedPubMedCentralCrossRefGoogle Scholar
  103. 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):821–830PubMedGoogle Scholar
  104. 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):1676–1679PubMedCrossRefGoogle Scholar
  105. 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):290–300PubMedCrossRefGoogle Scholar
  106. 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 11:13PubMedPubMedCentralCrossRefGoogle Scholar
  107. Unsay JD, Cosentino K, Subburaj Y, Garcia-Saez AJ (2013) Cardiolipin effects on membrane structure and dynamics. Langmuir 29(51):15878–15887PubMedCrossRefGoogle Scholar
  108. 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–E1034PubMedPubMedCentralCrossRefGoogle Scholar
  109. 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):1067–1079PubMedCrossRefGoogle Scholar
  110. 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):453–463PubMedPubMedCentralCrossRefGoogle Scholar
  111. 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):e63683PubMedPubMedCentralCrossRefGoogle Scholar
  112. 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):700–704PubMedCrossRefGoogle Scholar
  113. 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):6865–6875PubMedPubMedCentralGoogle Scholar
  114. 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):7202–7205PubMedPubMedCentralCrossRefGoogle Scholar
  115. Zhang YM, Rock CO (2008) Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6(3):222–233PubMedCrossRefGoogle Scholar
  116. 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):3879–3890PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zieske K, Schwille P (2014) Reconstitution of self-organizing protein gradients as spatial cues in cell-free systems. eLife 3:e03949PubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of BiochemistryUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Department of Biomedical EngineeringUniversity of Wisconsin-MadisonMadisonUSA
  3. 3.Department of ChemistryUniversity of Wisconsin-MadisonMadisonUSA

Personalised recommendations