Focus on membrane differentiation and membrane domains in the prokaryotic cell

Journal of Molecular Microbiology and Biotechnology

Volumn 23, Issue 4-5, 2013, Pages 345-356

  Boekema, Egbert J ^a   Scheffers, Dirk Jan ^a   Van Bezouwen, Laura S ^a   Bolhuis, Henk ^b   Folea, I Mihaela ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

Bacteria; Electron microscopy; Membranes

Indexed keywords

CARDIOLIPIN; FLUORESCENT DYE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL ENDOSPORE; BACTERIAL MEMBRANE; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL DIVISION; CELL MEMBRANE; CELL ORGANELLE; CHROMATOPHORE; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; EUKARYOTE; HALOPHILIC ARCHAEON; LIPID RAFT; MAGNETOSOME; MEMBRANE DIFFERENTIATION; MEMBRANE STRUCTURE; MORPHOLOGY; NONHUMAN; PHOTOTROPHIC BACTERIUM; POLAR BODY; PROKARYOTIC CELL; PROTEIN LOCALIZATION; PURPLE MEMBRANE;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); EUKARYOTA; PHOTOBACTERIA; PROKARYOTA;

EID: 84881490681     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000351361     Document Type: Article

References (81)

1. Arechaga I, Miroux B, Karrasch S, Huijbregts R, de Kruijff B, Runswick MJ, Walker JE: Characterisation of new intracellular membranes in Escherichia coli accompanying large scale over-production of the b subunit of F 1 F 0 ATP synthase. FEBS Lett 2000; 482: 215-219.
2. Arias-Cartin R, Grimaldi S, Arnoux P, Guigliarelli B, Magalon A: Cardiolipin binding in bacterial respiratory complexes: structural and functional implications. Biochim Biophys Acta 2012; 1817: 1937-1949.
3. Arteni AA, Nowaczyk M, Lax J, Kouil R, Rögner M, Boekema EJ: Single particle electron microscopy in combination with mass spectrometry to investigate novel complexes of membrane proteins. J Struct Biol 2005; 149: 325-331.
4. Bahatyrova S, Frese RN, Siebert CA, Olsen JD, van der Werf, KO, van Grondelle R, Niederman RA, Bullough PA, Otto C, Hunter CN: The native architecture of a photosynthetic membrane. Nature 2004; 430: 1058-1062.
5. Barák I, Muchová K, Wilkinson AJ, O'Toole PJ, Pavlendová N: Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 2008; 68: 1315-1327.
6. Bazett-Jones DP: Electron spectroscopic imaging of chromatin and other nucleoprotein complexes. Electron Microsc Rev 1992; 5: 37-58.
7. Bernal P, Muñoz-Rojas J, Hurtado A, Ramos JL, Segura A: A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality. Environ Microbiol 2007; 9: 1135-1145.
8. Boekema EJ, Folea M, Kouil R: Single particle electron microscopy. Photosynthesis Res 2009; 102: 189-196.
9. Boonstra AF, Germeroth L, Boekema EJ: Structure of the light harvesting antenna from Rhodospirillum molischianum studied by electron microscopy. Biochim Biophys Acta 1994; 1184: 227-234.
10. Bowen CC, Jensen TE: Blue-green algae: fine structure of the gas vacuoles. Science 1965; 147: 1460-1462.
11. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH, Tainer JA: Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 2006; 23: 651-662.
12. Cronan JE, Vagelos PR: Metabolism and function of the membrane phospholipids of Escherichia coli . Biochim Biophys Acta 1972; 265: 25-60.
13. Dempwolff F, Moeller HM, Graumann PL: 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 2012; 194: 4652-4661.
14. Donnelly CJ, Fainzilber M, Twiss JL: Subcellular communication through RNA transport and localized protein synthesis. Traffic 2010; 11: 1498-1505.
15. Donovan C, Bramkamp, M: Characterization and subcellular localization of a bacterial flotillin homologue. Microbiology 2009; 155: 1786-1799.
16. Donovan C, Sieger B, Kramer R, Bramkamp M: A synthetic Escherichia coli system identifies a conserved origin tethering factor in Actinobacteria. Mol Microbiol 2012: 84: 105-116.
17. Dudkina NV, Kouil R, Peters K, Braun HP, Boekema EJ: Structure and function of mitochondrial supercomplexes. Biochim Biophys Acta 2010b;1797: 664-670.
18. Dudkina NV, Oostergetel GT, Braun HP, Boekema EJ: Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography. Biochim Biophys Acta 2010a;1797: 272-277.
19. Ebersold HR, Cordier JL, Lüthy P: Bacterial mesosomes: method dependent artifacts. Arch Microbiol 1981; 130: 19-22.
20. Folea IM, Zhang P, Aro EM, Boekema EJ: Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett 2008; 582: 1749-1754.
21. Fu C, Wang K, Gan L, Lanman J, Khayat R, Young MJ, Jensen GJ, Doerschuk PC, Johnson JE: In vivo assembly of an archaeal virus studied with whole-cell electron cryotomography. Structure 2010a;18: 1579-1586.
22. Fu G, Huang T, Buss J, Coltharp C, Hensel Z, Xiao J: In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS One 2010b;5:e12682.
23. Fuerst J: Intracellular compartmentation in planctomycetes. Annu Rev Microbiol 2005; 59: 299-328.
24. Fuhrmann E, Bultema JB, Kahmann U, Rupprecht E, Boekema EJ, Schneider D: The vesicle inducing protein 1 from Synechocystis sp. PCC 6803 organizes into diverse higher ordered ring structures. Mol Cell Biol 2009; 20: 4620-4628.
25. Gan L, Jensen GJ: Electron tomography of cells. Quart Rev Biophys 2012; 45: 27-56.
26. Govindarajan S, Nevo-Dinur K, Amster-Choder O: Compartmentalization and spatiotemporal organization of macromolecules in bacteria. FEMS Microbiol Rev 2012; 36: 1005-1022.
27. Greene SE, Komeili A: Biogenesis and subcellular organization of the magnetosome organelles of magnetotactic bacteria. Curr Opin Cell Biol 2012; 24: 490-495.
28. Haupts U, Tittor J, Oesterhelt D: Closing in on bacteriorhodopsin: progress in understanding the molecule. Ann Rev Biophys Biomol Struct 1999; 28: 367-399.
29. Huitema E, Pritchard S, Matteson D, Radhakrishnan SK, Viollier PH: Bacterial birth scar proteins mark future flagellum assembly site. Cell 2006; 124: 1025-1037.
30. Jain S, Mocicka KB, Bos MP, Pachulec E, Stuart MCA, Keegstra W, Boekema EJ, van der Does C: Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria . PLoS ONE 2011; 6:e16624.
31. Javor B, Requadt C, Stoeckenius W: Box-shaped halophilic bacteria. J Bacteriol 1982; 151: 1532-1542.
32. Jogler C, Wanner G, Kolinko S, Niebler M, Amann R, Petersen N, Kube M, Reinhardt R, Schüler D: Conservation of proteobacterial magnetosome genes and structures in an uncultivated member of the deep-branching Nitrospira phylum. Proc Natl Acad Sci USA 2011; 108: 1134-1139.
33. Jyothikumar V, Klanbut K, Tiong J: Cardiolipin synthase is required for Streptomyces coelicolor morphogenesis. Mol Microbiol 2012; 84: 181-197.
34. Kawai F, Shoda M, Harashima R, Sadaie Y, Hara, H, Matsumoto K: Cardiolipin domains in Bacillus subtilis marburg membranes. J Bacteriol 2004: 186: 1475-1483.
35. Komeili A, Li Z, Newman DK, Jensen GJ: Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 2006; 311: 242-245.
36. Koppelman CM, den Blaauwen TD, Duursma MC, Heeren RM, Nanninga N: Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 2001; 183: 6144-6147.
37. Lam H, Schofield WB, Jacobs-Wagner C: A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 2006; 124: 1011-1023.
38. Lenarcic R, Halbedel S, Visser L, Shaw M, Wu LJ, Errington J, Marenduzzo D, Hamoen LW: Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 2009; 28: 2272-2282.
39. Lomize MA, Lomize AL, Pogozheva ID, Mosberg HI: OPM: orientations of proteins in membranes database. Bioinformatics 2006; 22: 623-625.
40. López D, Kolter R: Functional microdomains in bacterial membranes. Genes Dev 2010; 24: 1893-1902.
41. Madigan MT, Martinko JM, Parker J: Brock Biology of Microorganisms, ed 10. Upper Saddle River, Pearson Education, 2003, p 67.
42. Matsumoto K, Kusaka J, Nishibori A, Hara H: Lipid domains in bacterial membranes. Mol Microbiol 2006; 61: 1110-1117.
43. McLuskey K, Prince SM, Cogdell RJ, Isaacs NW: The crystallographic structure of the B800-820 LH3 light-harvesting complex from the purple bacteria Rhodopseudomonas Acidophila strain 7050. Biochemistry 2001; 40: 8783-8789.
44. Mileykovskaya E, Dowhan W: Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange. J Bacteriol 2000; 182: 1172-1175.
45. Mileykovskaya E, Fishov I, Fu X, Corbin BD, Margolin W, Dowhan W: Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 2003; 278: 22193-22198.
46. Mileykovskaya E, Sun Q, Margolin W, Dowhan W: Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. J Bacteriol 1998; 80: 4252-4257.
47. Mukhopadhyay R, Huang KC, Wingreen NS: Lipid localization in bacterial cells through curvature-mediated microphase separation. Biophys J 2008; 95: 1034-1049.
48. Nanninga N: The mesosome of Bacillus subtilis as affected by chemical and physical fixation. J Cell Biol 1971; 48: 219-224.
49. Nevo-Dinur K, Govindarajan S, Amster-Choder Orna: Subcellular localization of RNA and proteins in prokaryotes. Trends Genet 2012; 283: 14-322.
50. Nishibori A, Kusaka J, Hara H, Umeda M, Matsumoto K: Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 2005; 187: 2163-2174.
51. Nordhues A, Schöttler MA, Unger AK, Geimer S, Schönfelder S, Schmollinger S, Rütgers M, Finazzi G, Soppa B, Sommer F, Mühlhaus T, Roach T, Krieger-Liszkay A, Lokstein H, Cres po JL, Schroda M: Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas . Plant Cell 2012; 24: 637-659.
52. Oesterhelt D, Stoeckenius W: Rhodopsin-like protein from the purple membrane of Halobacterium halobium . Nature New Biology 1971; 233: 149-152.
53. Oostergetel GT, van Amerongen H, Boekema EJ: The chlorosome: a prototype for efficient light harvesting in photosynthesis. Photosynth Res 2010; 104; 245-255.
54. Qian P, Bullough PA, Hunter N: Three-dimensional reconstruction of a membrane-bending complex: the RC-LH1-PufX core dimer of Rhodobacter sphaeroides. J Biol Chem 2008; 283: 14002-14011.
55. Qian P, Hunter CN, Bullough PA: The 8.5A projection structure of the core RC-LH1-PufX dimer of Rhodobacter sphaeroides . J Mol Biol 2005; 349: 948-960.
56. Richter K, Gnagi H, Dubochet J: A model for cryosectioning based on the morphology of vitrified ultrathin sections. J Microsc 1991; 163: 19-28.
57. Romantsov T, Battle AR, Hendel JL, Martinac B, Wood JM: Protein localization in Escherichia coli cells: comparison of the cytoplasmic membrane proteins ProP, LacY, ProW, AqpZ, MscS and MscL. J Bacteriol 2010; 192: 912-924.
58. Romantsov T, Helbig S, Culham DE, Gill C, Stalker L, Wood JM: Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli . Mol Microbiol 2007; 64: 1455-1465.
59. Rudner DZ, Losick R: Protein subcellular localization in bacteria. Cold Spring Harb Perspect Biol 2009; 2:a0003072009.
60. Sato S, Kawamoto J, Sato SB, Watanabe B, Hiratake J, Esaki N, Kurihara T: Occurrence of a bacterial membrane microdomain at the cell division site enriched in phospholipids with polyunsaturated hydrocarbon chains. J Biol Chem 2012; 287: 24113-24121.
61. Scheffel A, Gruska M, Faivre D, Linaroudis A, Plitzko JM, Schüler D: An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 2006; 440: 110-114.
62. Semchonok DA, Chauvin JP, Frese RN, Jungas C, Boekema EJ: Structure of the dimeric RCLH1-PufX complex from Rhodobaca bogoriensis investigated by electron microscopy. Phil Trans R Soc B 2012; 367: 3412-3419.
63. Shaner NC, Steinbach PA, Tsien RY: A guide to choosing fluorescent proteins. Nat Methods 2005; 2: 905-909.
64. Simons K, Ikonen E: Functional rafts in cell membranes. Nature 1997; 387: 569-572.
65. Singer SJ, Nicolson GL: The fluid mosaic model of the structure of cell membranes. Science 1972; 175: 720-731.
66. Sonenshein AL, Hoch JA, Losick R (eds): Bacillus subtilis and Other Gram-Positive Bacteria. Washington, American Society for Microbiology, 1993, pp 1-987.
67. Stoeckenius W, Rowen R: A morphological study of Halobacterium halobium and its lysis in media of low salt concentration. J Cell Biol 1967; 34: 365-393.
68. Swulius MT, Jensen GJ: The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-Terminal Yellow fluorescent protein tag. J Bacteriol 2012; 194: 6382-6386.
69. Szwedziak P, Wang Q, Freund SMV, Löwe J: FtsA forms actin-like protofilaments. EMBO J 2012; 31: 2249-2260.
70. Taniguchi Y, Choi PJ, Li GW, Chen H, Babu M, Hearn J, Emili A, Xie XS: Quantifying E. coli proteome and transcriptome with singlemolecule sensitivity in single cells. Science 2010; 329: 533-538.
71. Tsien RY: The green fluorescent protein. Ann Rev Biochem 1998; 67: 509-544.
72. Typas A, Banzhaf M, Gross CA, Vollmer W: From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 2012; 10: 123-136.
73. Unwin PNT, Henderson R: Molecular structure determination by electron microscopy of unstained crystalline specimens. J Mol Biol 1975; 94: 425-440.
74. Vothknecht UC, Otters S, Hennig R, Schneider D: Vipp1: a very important protein in plastids?!. J Exp Botany 2012; 63: 1699-1712.
75. Walsby AE: Gas vesicles. Microbiol Rev 1994; 58: 94-144.
76. Walsby AE: The mechanical-properties of the microcystis gas vesicle. J Gen Microbiol 1991; 137: 2401-2408.
77. Wanner G, Steiner R, Scheer H: A three-dimensional model of the photosynthetic membranes of Ectothiorhodospira halochloris . Arch Microbiol 1986; 146: 267-274.
78. Xia W, Dowhan W: In vivo evidence for the involvement of anionic phospholipids in initiation of DNA replication in Escherichia coli . Proc Natl Acad Sci USA 1995; 92: 783-787.
79. Yamaichi Y, Bruckner R, Ringgaard S, Möll A, Cameron DE, Briegel A, Jensen GJ, Davis BM, Waldor MK: A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev 2012; 26: 2348-2360.
80. Yepes A, Scheider J, Mielich B, Koch G, García-Betancur JC, Ramamurthi KS, Vlamakis H, López D: The biofilm formation defect of a Bacillus subtilis flotillin-defective mutant involves the protease FtsH. Mol Microbiol 2012; 86: 457-471.
81. Yeremenko N, Kouril R, Ihalainen JA, D'Haene S, van Oosterwijk N, Andrizhiyevskaya EG, Keegstra W, Dekker HL, Hagemann M, Boekema EJ, Matthijs HCP, Dekker JP: Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 2004; 43: 10308-10313.