Advertisement

The Journal of Membrane Biology

, Volume 250, Issue 4, pp 367–378 | Cite as

Functional Membrane Microdomains Organize Signaling Networks in Bacteria

  • Rabea M. Wagner
  • Lara Kricks
  • Daniel Lopez
Article

Abstract

Membrane organization is usually associated with the correct function of a number of cellular processes in eukaryotic cells as diverse as signal transduction, protein sorting, membrane trafficking, or pathogen invasion. It has been recently discovered that bacterial membranes are able to compartmentalize their signal transduction pathways in functional membrane microdomains (FMMs). In this review article, we discuss the biological significance of the existence of FMMs in bacteria and comment on possible beneficial roles that FMMs play on the harbored signal transduction cascades. Moreover, four different membrane-associated signal transduction cascades whose functions are linked to the integrity of FMMs are introduced, and the specific role that FMMs play in stabilizing and promoting interactions of their signaling components is discussed. Altogether, FMMs seem to play a relevant role in promoting more efficient activation of signal transduction cascades in bacterial cells and show that bacteria are more sophisticated organisms than previously appreciated.

Keywords

Membrane microdomains Bacterial membranes Signal transduction 

References

  1. Babuke T, Tikkanen R (2007) Dissecting the molecular function of reggie/flotillin proteins. Eur J Cell Biol 86:525–532PubMedCrossRefGoogle Scholar
  2. Bach JN, Bramkamp M (2013) Flotillins functionally organize the bacterial membrane. Mol Microbiol 88:1205–1217PubMedCrossRefGoogle Scholar
  3. Bach JN, Bramkamp M (2015) Dissecting the molecular properties of prokaryotic flotillins. PLoS One 10:e0116750PubMedPubMedCentralCrossRefGoogle Scholar
  4. Barak I, Muchova K (2013) The role of lipid domains in bacterial cell processes. Int J Mol Sci 14:4050–4065PubMedPubMedCentralCrossRefGoogle Scholar
  5. Baumgart T, Hammond AT, Sengupta P, Hess ST, Holowka DA, Baird BA, Webb WW (2007) Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc Natl Acad Sci U S A 104:3165–3170PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bieniossek C, Schalch T, Bumann M, Meister M, Meier R, Baumann U (2006) The molecular architecture of the metalloprotease FtsH. Proc Natl Acad Sci U S A 103:3066–3071PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bisicchia P, Lioliou E, Noone D, Salzberg LI, Botella E, Hubner S, Devine KM (2010) Peptidoglycan metabolism is controlled by the WalRK (YycFG) and PhoPR two-component systems in phosphate-limited Bacillus subtilis cells. Mol Microbiol 75:972–989PubMedCrossRefGoogle Scholar
  8. Botella E, Hubner S, Hokamp K, Hansen A, Bisicchia P, Noone D, Powell L, Salzberg LI, Devine KM (2011) Cell envelope gene expression in phosphate-limited Bacillus subtilis cells. Microbiology 157:2470–2484PubMedCrossRefGoogle Scholar
  9. Bramkamp M, Lopez D (2015) Exploring the existence of lipid rafts in bacteria. Microbiol Mol Biol Rev 79:81–100PubMedPubMedCentralCrossRefGoogle Scholar
  10. Branda SS, Gonzalez-Pastor JE, Dervyn E, Ehrlich SD, Losick R, Kolter R (2004) Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186:3970–3979PubMedPubMedCentralCrossRefGoogle Scholar
  11. Browman DT, Hoegg MB, Robbins SM (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17:394–402PubMedCrossRefGoogle Scholar
  12. Brown, DA (2002). Isolation and use of rafts. Curr Protoc Immunol Chapter 11:Unit 11 10Google Scholar
  13. Bryan SJ, Burroughs NJ, Evered C, Sacharz J, Nenninger A, Mullineaux CW, Spence EM (2011) Loss of the SPHF homologue Slr1768 leads to a catastrophic failure in the maintenance of thylakoid membranes in Synechocystis sp. PCC 6803. PLoS One 6:e19625PubMedPubMedCentralCrossRefGoogle Scholar
  14. Burmann F, Ebert N, van Baarle S, Bramkamp M (2011) A bacterial dynamin-like protein mediating nucleotide-independent membrane fusion. Mol Microbiol 79:1294–1304PubMedCrossRefGoogle Scholar
  15. Capra EJ, Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325–347PubMedPubMedCentralCrossRefGoogle Scholar
  16. Castilla-Llorente V, Salas M, Meijer WJ (2008) kinC/D-mediated heterogeneous expression of spo0A during logarithmical growth in Bacillus subtilis is responsible for partial suppression of phi 29 development. Mol Microbiol 68:1406–1417PubMedCrossRefGoogle Scholar
  17. Chan YH, Boxer SG (2007) Model membrane systems and their applications. Curr Opin Chem Biol 11:581–587PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chapman SA, Asthagiri AR (2009) Quantitative effect of scaffold abundance on signal propagation. Mol Syst Biol 5:313PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dempwolff F, Moller HM, Graumann PL (2012a) Synthetic motility and cell shape defects associated with deletions of flotillin/reggie paralogs in Bacillus subtilis and interplay of these proteins with NfeD proteins. J Bacteriol 194:4652–4661PubMedPubMedCentralCrossRefGoogle Scholar
  20. Dempwolff F, Wischhusen HM, Specht M, Graumann PL (2012b) The deletion of bacterial dynamin and flotillin genes results in pleiotrophic effects on cell division, cell growth and in cell shape maintenance. BMC Microbiol 12:298PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dempwolff F, Schmidt FK, Hervas AB, Stroh A, Rosch TC, Riese CN, Dersch S, Heimerl T, Lucena D, Hulsbusch N, Stuermer CA, Takeshita N, Fischer R, Eckhardt B, Graumann PL (2016) Super resolution fluorescence microscopy and tracking of bacterial flotillin (reggie) paralogs provide evidence for defined-sized protein microdomains within the bacterial membrane but absence of clusters containing detergent-resistant proteins. PLoS Genet 12:e1006116PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dermine JF, Duclos S, Garin J, St-Louis F, Rea S, Parton RG, Desjardins M (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J Biol Chem 276:18507–18512PubMedCrossRefGoogle Scholar
  23. Deuerling E, Mogk A, Richter C, Purucker M, Schumann W (1997) The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol 23:921–933PubMedCrossRefGoogle Scholar
  24. Devi SN, Vishnoi M, Kiehler B, Haggett L, Fujita M (2015) In vivo functional characterization of the transmembrane histidine kinase KinC in Bacillus subtilis. Microbiology 161:1092–1104PubMedCrossRefGoogle Scholar
  25. Dickens M, Rogers JS, Cavanagh J, Raitano A, Xia Z, Halpern JR, Greenberg ME, Sawyers CL, Davis RJ (1997) A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277:693–696PubMedCrossRefGoogle Scholar
  26. Diekmann Y, Pereira-Leal JB (2013) Evolution of intracellular compartmentalization. Biochem J 449:319–331PubMedCrossRefGoogle Scholar
  27. Donovan C, Bramkamp M (2009) Characterization and subcellular localization of a bacterial flotillin homologue. Microbiology 155:1786–1799PubMedCrossRefGoogle Scholar
  28. Doughty DM, Dieterle M, Sessions AL, Fischer WW, Newman DK (2014) Probing the subcellular localization of hopanoid lipids in bacteria using NanoSIMS. PLoS One 9:e84455PubMedPubMedCentralCrossRefGoogle Scholar
  29. Epand RM, Epand RF (2009) Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta 1788:289–294PubMedCrossRefGoogle Scholar
  30. Feng X, Hu Y, Zheng Y, Zhu W, Li K, Huang CH, Ko TP, Ren F, Chan HC, Nega M, Bogue S, Lopez D, Kolter R, Gotz F, Guo RT, Oldfield E (2014) Structural and functional analysis of Bacillus subtilis YisP reveals a role of its product in biofilm production. Chem Biol 21:1557–1563PubMedPubMedCentralCrossRefGoogle Scholar
  31. Fujita M, Gonzalez-Pastor JE, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187:1357–1368PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gabaldon T, Pittis AA (2015) Origin and evolution of metabolic sub-cellular compartmentalization in eukaryotes. Biochimie 119:262–268PubMedPubMedCentralCrossRefGoogle Scholar
  33. Heimesaat MM, Lugert R, Fischer A, Alutis M, Kuhl AA, Zautner AE, Tareen AM, Gobel UB, Bereswill S (2014) Impact of Campylobacter jejuni cj0268c knockout mutation on intestinal colonization, translocation, and induction of immunopathology in gnotobiotic IL-10 deficient mice. PLoS One 9:e90148PubMedPubMedCentralCrossRefGoogle Scholar
  34. Heptinstall S, Archibald AR, Baddiley J (1970) Teichoic acids and membrane function in bacteria. Nature 225:519–521PubMedCrossRefGoogle Scholar
  35. Hu Y, Jia S, Ren F, Huang CH, Ko TP, Mitchell DA, Guo RT, Zheng Y (2013) Crystallization and preliminary X-ray diffraction analysis of YisP protein from Bacillus subtilis subsp. subtilis strain 168. Acta Crystallogr Sect F 69:77–79CrossRefGoogle Scholar
  36. Hulett FM (1996) The signal-transduction network for Pho regulation in Bacillus subtilis. Mol Microbiol 19:933–939PubMedCrossRefGoogle Scholar
  37. Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59:211–231PubMedCrossRefGoogle Scholar
  38. Jabra-Rizk MA, Shirtliff M, James C, Meiller T (2006) Effect of farnesol on Candida dubliniensis biofilm formation and fluconazole resistance. FEMS Yeast Res 6:1063–1073PubMedCrossRefGoogle Scholar
  39. Kawai F, Shoda M, Harashima R, Sadaie Y, Hara H, Matsumoto K (2004) Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 186:1475–1483PubMedPubMedCentralCrossRefGoogle Scholar
  40. Keller H, Worch R, Schwille P (2013) Model membrane systems. Methods Mol Biol 1008:417–438PubMedCrossRefGoogle Scholar
  41. Kihara A, Akiyama Y, Ito K (1996) A protease complex in the Escherichia coli plasma membrane: HflKC (HflA) forms a complex with FtsH (HflB), regulating its proteolytic activity against SecY. EMBO J 15:6122–6131PubMedPubMedCentralGoogle Scholar
  42. Langhorst MF, Reuter A, Stuermer CA (2005) Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell Mol Life Sci 62:2228–2240PubMedCrossRefGoogle Scholar
  43. Le AT, Schumann W (2009) The Spo0E phosphatase of Bacillus subtilis is a substrate of the FtsH metalloprotease. Microbiology 155:1122–1132PubMedCrossRefGoogle Scholar
  44. LeDeaux JR, Grossman AD (1995) Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis. J Bacteriol 177:166–175PubMedPubMedCentralCrossRefGoogle Scholar
  45. Levchenko A, Bruck J, Sternberg PW (2000) Scaffold proteins may biphasically affect the levels of mitogen-activated protein kinase signaling and reduce its threshold properties. Proc Natl Acad Sci U S A 97:5818–5823PubMedPubMedCentralCrossRefGoogle Scholar
  46. Levental KR, Levental I (2015a) Giant plasma membrane vesicles: models for understanding membrane organization. Curr Top Membr 75:25–57PubMedCrossRefGoogle Scholar
  47. Levental KR, Levental I (2015b) Isolation of giant plasma membrane vesicles for evaluation of plasma membrane structure and protein partitioning. Methods Mol Biol 1232:65–77PubMedCrossRefGoogle Scholar
  48. Levental I, Lingwood D, Grzybek M, Coskun U, Simons K (2010) Palmitoylation regulates raft affinity for the majority of integral raft proteins. Proc Natl Acad Sci U S A 107:22050–22054PubMedPubMedCentralCrossRefGoogle Scholar
  49. Liu W, Hulett FM (1998) Comparison of PhoP binding to the tuaA promoter with PhoP binding to other Pho-regulon promoters establishes a Bacillus subtilis Pho core binding site. Microbiology 144(Pt 5):1443–1450PubMedCrossRefGoogle Scholar
  50. Liu W, Eder S, Hulett FM (1998) Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role for PhoP-P. J Bacteriol 180:753–758PubMedPubMedCentralGoogle Scholar
  51. Lopez D (2015) Molecular composition of functional microdomains in bacterial membranes. Chem Phys Lipids 192:3–11PubMedCrossRefGoogle Scholar
  52. Lopez D, Kolter R (2010a) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34:134–149PubMedCrossRefGoogle Scholar
  53. Lopez D, Kolter R (2010b) Functional microdomains in bacterial membranes. Genes Dev 24:1893–1902PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lopez D, Fischbach MA, Chu F, Losick R, Kolter R (2009a) Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc Natl Acad Sci U S A 106:280–285PubMedCrossRefGoogle Scholar
  55. Lopez D, Vlamakis H, Losick R, Kolter R (2009b) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74:609–618PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lopez D, Vlamakis H, Kolter R (2010) Biofilms. Cold Spring Harb Perspect. Biol 2:a000398Google Scholar
  57. Maddock JR, Shapiro L (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259:1717–1723PubMedCrossRefGoogle Scholar
  58. Mascher T, Helmann JD, Unden G (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70:910–938PubMedPubMedCentralCrossRefGoogle Scholar
  59. Matsumoto K, Kusaka J, Nishibori A, Hara H (2006) Lipid domains in bacterial membranes. Mol Microbiol 61:1110–1117PubMedCrossRefGoogle Scholar
  60. McLoon AL, Kolodkin-Gal I, Rubinstein SM, Kolter R, Losick R (2011) Spatial regulation of histidine kinases governing biofilm formation in Bacillus subtilis. J Bacteriol 193:679–685PubMedCrossRefGoogle Scholar
  61. Michel V, Bakovic M (2007) Lipid rafts in health and disease. Biol Cell 99:129–140PubMedCrossRefGoogle Scholar
  62. Mielich-Suss B, Schneider J, Lopez D (2013) Overproduction of flotillin influences cell differentiation and shape in Bacillus subtilis. MBio 4:e00719PubMedPubMedCentralCrossRefGoogle 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 182:1172–1175PubMedPubMedCentralCrossRefGoogle Scholar
  64. 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 507:187–190PubMedCrossRefGoogle Scholar
  65. Miller LJ, Ray LB (1992) Cellular membranes. Science 258:871PubMedCrossRefGoogle Scholar
  66. Mishra S, Joshi PG (2007) Lipid raft heterogeneity: an enigma. J Neurochem 103(Suppl 1):135–142PubMedCrossRefGoogle Scholar
  67. Muller JP, An Z, Merad T, Hancock IC, Harwood CR (1997) Influence of Bacillus subtilis phoR on cell wall anionic polymers. Microbiology 143(Pt 3):947–956PubMedCrossRefGoogle Scholar
  68. Nakano MM, Zuber P, Glaser P, Danchin A, Hulett FM (1996) Two-component regulatory proteins ResD-ResE are required for transcriptional activation of fnr upon oxygen limitation in Bacillus subtilis. J Bacteriol 178:3796–3802PubMedPubMedCentralCrossRefGoogle Scholar
  69. Neumann AK, Itano MS, Jacobson K (2010) Understanding lipid rafts and other related membrane domains. F1000 Biol Rep 2:31PubMedPubMedCentralCrossRefGoogle Scholar
  70. Neumann-Giesen C, Falkenbach B, Beicht P, Claasen S, Luers G, Stuermer CA, Herzog V, Tikkanen R (2004) Membrane and raft association of reggie-1/flotillin-2: role of myristoylation, palmitoylation and oligomerization and induction of filopodia by overexpression. Biochem J 378:509–518PubMedPubMedCentralCrossRefGoogle Scholar
  71. Otto GP, Nichols BJ (2011) The roles of flotillin microdomains–endocytosis and beyond. J Cell Sci 124:3933–3940PubMedCrossRefGoogle Scholar
  72. Reith J, Mayer C (2011) Peptidoglycan turnover and recycling in Gram-positive bacteria. Appl Microbiol Biotechnol 92:1–11PubMedCrossRefGoogle Scholar
  73. Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A 107:2230–2234PubMedPubMedCentralCrossRefGoogle Scholar
  74. Saenz JP, Sezgin E, Schwille P, Simons K (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci U S A 109:14236–14240PubMedPubMedCentralCrossRefGoogle Scholar
  75. Saenz JP, Grosser D, Bradley AS, Lagny TJ, Lavrynenko O, Broda M, Simons K (2015) Hopanoids as functional analogues of cholesterol in bacterial membranes. Proc Natl Acad Sci U S A 112:11971–11976PubMedPubMedCentralCrossRefGoogle Scholar
  76. Salazar ME, Laub MT (2015) Temporal and evolutionary dynamics of two-component signaling pathways. Curr Opin Microbiol 24:7–14PubMedPubMedCentralCrossRefGoogle Scholar
  77. Santos D, De Almeida DF (1975) Isolation and characterization of a new temperature-sensitive cell division mutant of Escherichia coli K-12. J Bacteriol 124:1502–1507PubMedPubMedCentralGoogle Scholar
  78. Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:402PubMedPubMedCentralCrossRefGoogle Scholar
  79. Sawant P, Eissenberger K, Karier L, Mascher T, Bramkamp M (2015) A dynamin-like protein involved in bacterial cell membrane surveillance under environmental stress. Environ Microbiol (in press)Google Scholar
  80. Scheffers DJ, Pinho MG (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69:585–607PubMedPubMedCentralCrossRefGoogle Scholar
  81. Schneider J, Klein T, Mielich-Suss B, Koch G, Franke C, Kuipers OP, Kovacs AT, Sauer M, Lopez D (2015a) Spatio-temporal remodeling of functional membrane microdomains organizes the signaling networks of a bacterium. PLoS Genet 11:e1005140PubMedPubMedCentralCrossRefGoogle Scholar
  82. Schneider J, Mielich-Suss B, Bohme R, Lopez D (2015b) In vivo characterization of the scaffold activity of flotillin on the membrane kinase KinC of Bacillus subtilis. Microbiology 161:1871–1887PubMedPubMedCentralCrossRefGoogle Scholar
  83. Schumann W (1999) FtsH–a single-chain charonin? FEMS Microbiol Rev 23:1–11PubMedCrossRefGoogle Scholar
  84. Scott RE (1976) Plasma membrane vesiculation: a new technique for isolation of plasma membranes. Science 194:743–745PubMedCrossRefGoogle Scholar
  85. Sezgin E, Schwille P (2012) Model membrane platforms to study protein-membrane interactions. Mol Membr Biol 29:144–154PubMedCrossRefGoogle Scholar
  86. Sezgin E, Kaiser HJ, Baumgart T, Schwille P, Simons K, Levental I (2012a) Elucidating membrane structure and protein behavior using giant plasma membrane vesicles. Nat Protoc 7:1042–1051PubMedCrossRefGoogle Scholar
  87. Sezgin E, Levental I, Grzybek M, Schwarzmann G, Mueller V, Honigmann A, Belov VN, Eggeling C, Coskun U, Simons K, Schwille P (2012b) Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes. Biochim Biophys Acta 1818:1777–1784PubMedCrossRefGoogle Scholar
  88. Shemesh M, Kolter R, Losick R (2010) The biocide chlorine dioxide stimulates biofilm formation in Bacillus subtilis by activation of the histidine kinase KinC. J Bacteriol 192:6352–6356PubMedPubMedCentralCrossRefGoogle Scholar
  89. Simons K, Gerl MJ (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11:688–699PubMedCrossRefGoogle Scholar
  90. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572PubMedCrossRefGoogle Scholar
  91. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731PubMedCrossRefGoogle Scholar
  92. Somani VK, Aggarwal S, Singh D, Prasad T, Bhatnagar R (2016) Identification of Novel Raft Marker Protein, FlotP in Bacillus anthracis. Front Microbiol 7:169PubMedPubMedCentralCrossRefGoogle Scholar
  93. Stock JB, Levit MN, Wolanin PM (2002) Information processing in bacterial chemotaxis. Sci STKE 2002:pe25Google Scholar
  94. Strahl H, Ronneau S, Gonzalez BS, Klutsch D, Schaffner-Barbero C, Hamoen LW (2015) Transmembrane protein sorting driven by membrane curvature. Nat Commun 6:8728PubMedPubMedCentralCrossRefGoogle Scholar
  95. Stuermer CA (2010) The reggie/flotillin connection to growth. Trends Cell Biol 20:6–13PubMedCrossRefGoogle Scholar
  96. Stuermer CA, Plattner H (2005) The ‘lipid raft’ microdomain proteins reggie-1 and reggie-2 (flotillins) are scaffolds for protein interaction and signalling. Biochem Soc Symp 72:109–118CrossRefGoogle Scholar
  97. Sun G, Birkey SM, Hulett FM (1996) Three two-component signal-transduction systems interact for Pho regulation in Bacillus subtilis. Mol Microbiol 19:941–948PubMedCrossRefGoogle Scholar
  98. Tareen AM, Luder CG, Zautner AE, Grobeta U, Heimesaat MM, Bereswill S, Lugert R (2013) The Campylobacter jejuni Cj0268c protein is required for adhesion and invasion in vitro. PLoS One 8:e81069PubMedPubMedCentralCrossRefGoogle Scholar
  99. Tavernarakis N, Driscoll M, Kyrpides NC (1999) The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends Biochem Sci 24:425–427PubMedCrossRefGoogle Scholar
  100. Toledo A, Perez A, Coleman JL, Benach JL (2015) The lipid raft proteome of Borrelia burgdorferi. Proteomics 15:3662–3675PubMedCrossRefGoogle Scholar
  101. Typas A, Banzhaf M, Gross CA, Vollmer W (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10:123–136Google Scholar
  102. 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 49:1067–1079PubMedCrossRefGoogle Scholar
  103. Veening JW, Hamoen LW, Kuipers OP (2005) Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis. Mol Microbiol 56:1481–1494PubMedCrossRefGoogle Scholar
  104. Vollmer W, Bertsche U (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778:1714–1734PubMedCrossRefGoogle Scholar
  105. Vollmer W, Blanot D, de Pedro MA (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32:149–167PubMedCrossRefGoogle Scholar
  106. Welander PV, Hunter RC, Zhang L, Sessions AL, Summons RE, Newman DK (2009) Hopanoids play a role in membrane integrity and pH homeostasis in Rhodopseudomonas palustris TIE-1. J Bacteriol 191:6145–6156PubMedPubMedCentralCrossRefGoogle Scholar
  107. White DC, Frerman FE (1967) Extraction, characterization, and cellular localization of the lipids of Staphylococcus aureus. J Bacteriol 94:1854–1867PubMedPubMedCentralGoogle Scholar
  108. Wolanin PM, Thomason PA, Stock JB (2002) Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biol 3(10):1 REVIEWS3013 CrossRefGoogle Scholar
  109. Yepes A, Schneider J, Mielich B, Koch G, Garcia-Betancur JC, Ramamurthi KS, Vlamakis H, Lopez D (2012) The biofilm formation defect of a Bacillus subtilis flotillin-defective mutant involves the protease FtsH. Mol Microbiol 86:457–471PubMedPubMedCentralCrossRefGoogle Scholar
  110. Yokoyama H, Fujii S, Matsui I (2008) Crystal structure of a core domain of stomatin from Pyrococcus horikoshii Illustrates a novel trimeric and coiled-coil fold. J Mol Biol 376:868–878PubMedCrossRefGoogle Scholar
  111. Zeke A, Lukacs M, Lim WA, Remenyi A (2009) Scaffolds: interaction platforms for cellular signalling circuits. Trends Cell Biol 19:364–374PubMedPubMedCentralCrossRefGoogle Scholar
  112. Zhang HM, Li Z, Tsudome M, Ito S, Takami H, Horikoshi K (2005) An alkali-inducible flotillin-like protein from Bacillus halodurans C-125. Protein J 24:125–131PubMedCrossRefGoogle Scholar
  113. Zhao F, Zhang J, Liu YS, Li L, He YL (2011) Research advances on flotillins. Virol J 8:479PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Rabea M. Wagner
    • 1
    • 2
    • 3
  • Lara Kricks
    • 1
    • 2
    • 3
  • Daniel Lopez
    • 1
    • 2
    • 3
  1. 1.Research Centre for Infectious Diseases (ZINF)University of WürzburgWürzburgGermany
  2. 2.Institute for Molecular Infection Biology (IMIB)University of WürzburgWürzburgGermany
  3. 3.National Center for Biotechnology (CNB), Spanish Research Council (CSIC)Universidad Autonoma de MadridMadridSpain

Personalised recommendations