1887

Abstract

The outer membrane of Gram-negative bacteria is an essential compartment containing a specific complement of lipids and proteins that constitute a protective, selective permeability barrier. Outer membrane -barrel proteins are assembled into the membrane by the essential hetero-oligomeric BAM complex, which contains the lipoprotein BamE. We have identified a homologue of BamE, encoded by , which is located in the outer membrane of the stalked alpha-proteobacterium . BamE associates with proteins whose homologues in other bacteria are known to participate in outer membrane protein assembly: BamA (CC1915), BamB (CC1653) and BamD (CC1984). cells lacking BamE grow slowly in rich medium and are hypersensitive to anionic detergents, some antibiotics and heat exposure, which suggest that the membrane integrity of the mutant is compromised. Membranes of the Δ mutant have normal amounts of the outer membrane protein RsaF, a TolC homologue, but are deficient in CpaC*, an aggregated form of the outer membrane secretin for type IV pili. Δ membranes also contain greatly reduced amounts of three TonB-dependent receptors that are abundant in wild-type cells. Cells lacking BamE have short stalks and are delayed in stalk outgrowth during the cell cycle. Based on these findings, we propose that BamE participates in the assembly of outer membrane -barrel proteins, including one or more substrates required for the initiation of stalk biogenesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.035055-0
2010-03-01
2019-11-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/3/742.html?itemId=/content/journal/micro/10.1099/mic.0.035055-0&mimeType=html&fmt=ahah

References

  1. Alley, M. R., Maddock, J. R. & Shapiro, L. ( 1992; ). Polar localization of a bacterial chemoreceptor. Genes Dev 6, 825–836.[CrossRef]
    [Google Scholar]
  2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman,D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  3. Alvarez-Martinez, C. E., Baldini, R. L. & Gomes, S. L. ( 2006; ). A Caulobacter crescentus extracytoplasmicfunction sigma factor mediating the response to oxidative stress in stationaryphase. J Bacteriol 188, 1835–1846.[CrossRef]
    [Google Scholar]
  4. Alvarez-Martinez, C. E., Lourenco, R. F., Baldini, R. L., Laub,M. T. & Gomes, S. L. ( 2007; ). The ECF sigma factor σ T is involved in osmotic and oxidative stress responsesin Caulobacter crescentus. Mol Microbiol 66, 1240–1255.[CrossRef]
    [Google Scholar]
  5. Badger, J. H., Hoover, T. R., Brun, Y. V., Weiner, R. M., Laub,M. T., Alexandre, G., Mrázek, J., Ren, Q., Paulsen, I. T. & otherauthors ( 2006; ). Comparative genomic evidence for aclose relationship between the dimorphic prosthecate bacteria Hyphomonasneptunium and Caulobacter crescentus. J Bacteriol 188, 6841–6850.[CrossRef]
    [Google Scholar]
  6. Bassford, P. J., Jr & Kadner, R. J. ( 1977; ). Genetic analysis of components involved in vitamin B12 uptake in Escherichia coli. J Bacteriol 132, 796–805.
    [Google Scholar]
  7. Bayan, N., Guilvout, I. & Pugsley, A. P. ( 2006; ). Secretins take shape. Mol Microbiol 60, 1–4.[CrossRef]
    [Google Scholar]
  8. Biondi, E. G., Skerker, J. M., Arif, M., Prasol, M. S., Perchuk,B. S. & Laub, M. T. ( 2006; ). A phosphorelay systemcontrols stalk biogenesis during cell cycle progression in Caulobactercrescentus. Mol Microbiol 59, 386–401.[CrossRef]
    [Google Scholar]
  9. Blanvillain, S., Meyer, D., Boulanger, A., Lautier, M., Guynet,C., Denance, N., Vasse, J., Lauber, E. & Arlat, M. ( 2007; ). Plant carbohydrate scavenging through TonB-dependent receptors:a feature shared by phytopathogenic and aquatic bacteria. PLoSOne 2, e224
    [Google Scholar]
  10. Bouvier, J., Pugsley, A. P. & Stragier, P. ( 1991; ). A gene for a new lipoprotein in the dapA–purC interval of the Escherichia coli chromosome. J Bacteriol 173, 5523–5531.
    [Google Scholar]
  11. Braun, V. & Endriss, F. ( 2007; ).Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 20, 219–231.[CrossRef]
    [Google Scholar]
  12. Brun, Y. V. & Shapiro, L. ( 1992; ).A temporally controlled sigma-factor is required for polar morphogenesis andnormal cell division in Caulobacter. Genes Dev 6, 2395–2408.[CrossRef]
    [Google Scholar]
  13. Charlson, E. S., Werner, J. N. & Misra, R. ( 2006; ). Differential effects of yfgL mutation on Escherichiacoli outer membrane proteins and lipopolysaccharide. J Bacteriol 188, 7186–7194.[CrossRef]
    [Google Scholar]
  14. Clancy, M. J. & Newton, A. ( 1982; ).Localization of proteins in the inner and outer membranes of Caulobactercrescentus. Biochim Biophys Acta 686, 160–169.[CrossRef]
    [Google Scholar]
  15. Collier, J. & Shapiro, L. ( 2007; ).Spatial complexity and control of a bacterial cell cycle. CurrOpin Biotechnol 18, 333–340.
    [Google Scholar]
  16. Collin, S., Guilvout, I., Chami, M. & Pugsley, A. P. ( 2007; ). YaeT-independent multimerization and outer membraneassociation of secretin PulD. Mol Microbiol 64, 1350–1357.[CrossRef]
    [Google Scholar]
  17. Dartigalongue, C., Missiakas, D. & Raina, S. ( 2001; ). Characterization of the Escherichia coli sigmaE regulon. J Biol Chem 276, 20866–20875.[CrossRef]
    [Google Scholar]
  18. Delcour, A. H. ( 2002; ). Structure andfunction of pore-forming β-barrels from bacteria. J Mol Microbiol Biotechnol 4, 1–10.
    [Google Scholar]
  19. DelVecchio, V. G., Kapatral, V., Elzer, P., Patra, G. &Mujer, C. V. ( 2002; ). The genome of Brucella melitensis. Vet Microbiol 90, 587–592.[CrossRef]
    [Google Scholar]
  20. Doerrler, W. T. & Raetz, C. R. ( 2005; ). Loss of outer membrane proteins without inhibition of lipid export inan Escherichia coli YaeT mutant. J Biol Chem 280, 27679–27687.[CrossRef]
    [Google Scholar]
  21. Elias, J. E., Haas, W., Faherty, B. K. & Gygi, S. P. ( 2005; ). Comparative evaluation of mass spectrometry platformsused in large-scale proteomics investigations. Nat Methods 2, 667–675.[CrossRef]
    [Google Scholar]
  22. Ely, B. ( 1991; ). Genetics of Caulobactercrescentus. Methods Enzymol 204, 372–384.
    [Google Scholar]
  23. Eng, J. K., McCormack, A. L. & Yates, J. R., III ( 1994; ). An approach to correlate tandem mass spectral dataof peptides with amino acid sequences in a protein database. JAm Soc Mass Spectrom 5, 976–989.
    [Google Scholar]
  24. Evinger, M. & Agabian, N. ( 1977; ).Envelope-associated nucleoid from Caulobacter crescentus stalkedand swarmer cells. J Bacteriol 132, 294–301.
    [Google Scholar]
  25. Fardini, Y., Trotereau, J., Bottreau, E., Souchard, C., Velge,P. & Virlogeux-Payant, I. ( 2009; ). Investigationof the role of the BAM complex and SurA chaperone in outer-membrane proteinbiogenesis and type III secretion system expression in Salmonella. Microbiology 155, 1613–1622.[CrossRef]
    [Google Scholar]
  26. Fuangthong, M., Sallabhan, R., Atichartpongkul, S., Rangkadilok,N., Sriprang, R., Satayavivad, J. & Mongkolsuk, S. ( 2008; ). The omlA gene is involved in multidrug resistance andits expression is inhibited by coumarins in Xanthomonas campestrispv. phaseoli. Arch Microbiol 189, 211–218.[CrossRef]
    [Google Scholar]
  27. Gatsos, X., Perry, A. J., Anwari, K., Dolezal, P., Wolynec,P. P., Likic, V. A., Purcell, A. W., Buchanan, S. K. & Lithgow, T. ( 2008; ). Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiol Rev 32, 995–1009.[CrossRef]
    [Google Scholar]
  28. Gonin, M., Quardokus, E. M., O'Donnol, D., Maddock, J. &Brun, Y. V. ( 2000; ). Regulation of stalk elongationby phosphate in Caulobacter crescentus. J Bacteriol 182, 337–347.[CrossRef]
    [Google Scholar]
  29. Grizot, S. & Buchanan, S. K. ( 2004; ). Structure of the OmpA-like domain of RmpM from Neisseria meningitidis. Mol Microbiol 51, 1027–1037.[CrossRef]
    [Google Scholar]
  30. Habib, S. J., Waizenegger, T., Niewienda, A., Paschen, S. A.,Neupert, W. & Rapaport, D. ( 2007; ). The N-terminaldomain of Tob55 has a receptor-like function in the biogenesis of mitochondrial β-barrel proteins. J Cell Biol 176, 77–88.[CrossRef]
    [Google Scholar]
  31. House, B. L., Mortimer, M. W. & Kahn, M. L. ( 2004; ). New recombination methods for Sinorhizobium meliloti genetics. Appl Environ Microbiol 70, 2806–2815.[CrossRef]
    [Google Scholar]
  32. Iba, H., Fukuda, A. & Okada, Y. ( 1977; ). Chromosome replication in Caulobacter crescentus growing ina nutrient broth. J Bacteriol 129, 1192–1197.
    [Google Scholar]
  33. Ireland, M. M. E., Karty, J. A., Quardokus, E. M., Reilly, J.P. & Brun, Y. V. ( 2002; ). Proteomic analysis ofthe Caulobacter crescentus stalk indicates competence for nutrientuptake. Mol Microbiol 45, 1029–1041.[CrossRef]
    [Google Scholar]
  34. Jansen, C., Wiese, A., Reubsaet, L., Dekker, N., de Cock, H.,Seydel, U. & Tommassen, J. ( 2000; ). Biochemicaland biophysical characterization of in vitro folded outer membraneporin PorA of Neisseria meningitidis. Biochim BiophysActa 1464, 284–298.
    [Google Scholar]
  35. Jimenez, C. R., Huang, L., Qiu, Y. & Burlingame, A. L. ( 1998; ). In-gel digestion of proteins for MALDI-MS fingerprintmapping. In Current Protocols in Protein Science, pp. 16.14.11–16.14.15.Edited by J. E. Coligan, B. M. Dunn, H. L. Ploegh, D. W. Speicher & P.T. Wingfield. New York: Wiley.
  36. Kabir, M. S., Yamashita, D., Koyama, S., Oshima, T., Kurokawa,K., Maeda, M., Tsunedomi, R., Murata, M., Wada, C. & other authors ( 2005; ). Cell lysis directed by σ Ein early stationary phase and effect of induction of the rpoE geneon global gene expression in Escherichia coli. Microbiology 151, 2721–2735.[CrossRef]
    [Google Scholar]
  37. Kainth, P. & Gupta, R. S. ( 2005; ).Signature proteins that are distinctive of alpha proteobacteria. BMC Genomics 6, 94 [CrossRef]
    [Google Scholar]
  38. Knowles, T. J., Jeeves, M., Bobat, S., Dancea, F., McClelland,D., Palmer, T., Overduin, M. & Henderson, I. R. ( 2008; ). Fold and function of polypeptide transport-associated domains responsiblefor delivering unfolded proteins to membranes. Mol Microbiol 68, 1216–1227.[CrossRef]
    [Google Scholar]
  39. Knowles, T. J., Scott-Tucker, A., Overduin, M. & Henderson,I. R. ( 2009; ). Membrane protein architects: the roleof the BAM complex in outer membrane protein assembly. Nat RevMicrobiol 7, 206–214.
    [Google Scholar]
  40. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B. & Hughes,C. ( 2000; ). Crystal structure of the bacterial membraneprotein TolC central to multidrug efflux and protein export. Nature 405, 914–919.[CrossRef]
    [Google Scholar]
  41. Koronakis, V., Eswaran, J. & Hughes, C. ( 2004; ). Structure and function of TolC: the bacterial exit duct forproteins and drugs. Annu Rev Biochem 73, 467–489.[CrossRef]
    [Google Scholar]
  42. Lassmann, T. & Sonnhammer, E. L. L. ( 2005; ). Kalign – an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6, 298 [CrossRef]
    [Google Scholar]
  43. Lewenza, S., Vidal-Ingigliardi, D. & Pugsley, A. P. ( 2006; ). Direct visualization of red fluorescent lipoproteinsindicates conservation of the membrane sorting rules in the family Enterobacteriaceae. J Bacteriol 188, 3516–3524.[CrossRef]
    [Google Scholar]
  44. Lewis, C., Skovierova, H., Rowley, G., Rezuchova, B., Homerova,D., Stevenson, A., Sherry, A., Kormanec, J. & Roberts, M. ( 2008; ). Small outer-membrane protein lipoprotein, SmpA, is regulatedby σ E and has a role in cell envelope integrity andvirulence of Salmonella enterica serovar Typhimurium. Microbiology 154, 979–988.[CrossRef]
    [Google Scholar]
  45. Malinverni, J. C., Werner, J., Kim, S., Sklar, J. G., Kahne,D., Misra, R. & Silhavy, T. J. ( 2006; ). YfiO stabilizesthe YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61, 151–164.[CrossRef]
    [Google Scholar]
  46. McLeod, M., Craft, S. & Broach, J. R. ( 1986; ). Identification of the crossover site during FLP-mediated recombinationin the Saccharomyces cerevisiae plasmid  μ circle. Mol Cell Biol 6, 3357–3367.
    [Google Scholar]
  47. Molloy, M. P., Phadke, N. D., Maddock, J. R. & Andrews,P. C. ( 2001; ). Two-dimensional electrophoresis andpeptide mass fingerprinting of bacterial outer membrane proteins. Electrophoresis 22, 1686–1696.[CrossRef]
    [Google Scholar]
  48. Narita, S. & Tokuda, H. ( 2007; ).Amino acids at positions 3 and 4 determine the membrane specificity of Pseudomonas aeruginosa lipoproteins. J Biol Chem 282, 13372–13378.[CrossRef]
    [Google Scholar]
  49. Narita, S., Matsuyama, S. & Tokuda, H. ( 2004; ). Lipoprotein trafficking in Escherichia coli. Arch Microbiol 182, 1–6.[CrossRef]
    [Google Scholar]
  50. Neugebauer, H., Herrmann, C., Kammer, W., Schwartz, G., Nordheim,A. & Braun, V. ( 2005; ). ExbBD-dependent transportof maltodextrins through the novel MalA protein across the outer membraneof Caulobacter crescentus. J Bacteriol 187, 8300–8311.[CrossRef]
    [Google Scholar]
  51. Nierman, W. C., Feldblyum, T. V., Laub, M. T., Paulsen, I. T.,Nelson, K. E., Eisen, J. A., Heidelberg, J. F., Alley, M. R., Ohta, N. &other authors ( 2001; ). Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci U S A 98, 4136–4141.[CrossRef]
    [Google Scholar]
  52. Nikaido, H. ( 2003; ). Molecular basisof bacterial outer membrane permeability revisited. Microbiol MolBiol Rev 67, 593–656.
    [Google Scholar]
  53. Ochsner, U. A., Vasil, A. I., Johnson, Z. & Vasil, M. I. ( 1999; ). Pseudomonas aeruginosa fur overlapswith a gene encoding a novel outer membrane lipoprotein, OmlA. J Bacteriol 181, 1099–1109.
    [Google Scholar]
  54. Phadke, N. D., Molloy, M. P., Steinhoff, S. A., Ulintz, P. J.,Andrews, P. C. & Maddock, J. R. ( 2001; ). Analysisof the outer membrane proteome of Caulobacter crescentus by two-dimensionalelectrophoresis and mass spectrometry. Proteomics 1, 705–720.[CrossRef]
    [Google Scholar]
  55. Poindexter, J. S. ( 1964; ). Biologicalproperties and classification of the Caulobacter group. Bacteriol Rev 28, 231–295.
    [Google Scholar]
  56. Poindexter, J. L. S. & Cohen-Bazire, G. ( 1964; ). The fine structure of stalked bacteria belonging to the family Caulobacteraceae. J Cell Biol 23, 587–607.[CrossRef]
    [Google Scholar]
  57. Postle, K. & Larsen, R. A. ( 2007; ).TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20, 453–465.[CrossRef]
    [Google Scholar]
  58. Prinz, T. & Tommassen, J. ( 2000; ).Association of iron-regulated outer membrane proteins of Neisseria meningitidis with RmpM (class 4) protein. FEMS Microbiol Lett 183, 49–53.[CrossRef]
    [Google Scholar]
  59. Pugsley, A. P. & Reeves, R. ( 1976; ). Iron uptake in colicin B-resistance mutants of Escherichia coliK-12. J Bacteriol 126, 1052–1062.
    [Google Scholar]
  60. Quon, K. C., Marczynski, G. T. & Shapiro, L. ( 1996; ). Cell cycle control by an essential bacterial two-componentsignal transduction protein. Cell 84, 83–93.[CrossRef]
    [Google Scholar]
  61. Raleigh, E. A., Elbing, K. & Brent, R. ( 2002; ). Selected topics from classical bacterial genetics. In CurrentProtocols in Molecular Biology, pp. 1.4.1–1.4.14. Edited by F.M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith &K. Struhl. New York: Wiley.
  62. Reisinger, S. J., Huntwork, S., Viollier, P. H. & Ryan,K. R. ( 2007; ). DivL performs critical cell cycle functionsin Caulobacter crescentus independent of kinase activity. J Bacteriol 189, 8308–8320.[CrossRef]
    [Google Scholar]
  63. Rezuchova, B., Miticka, H., Homerova, D., Roberts, M. &Kormanec, J. ( 2003; ). New members of the Escherichiacoli σ E regulon identified by a two-plasmid system. FEMS Microbiol Lett 225, 1–7.[CrossRef]
    [Google Scholar]
  64. Robert, V., Volokhina, E. B., Senf, F., Bos, M. P., Van Gelder,P. & Tommassen, J. ( 2006; ). Assembly factor Omp85recognizes its outer membrane protein substrates by a species-specific C-terminalmotif. PLoS Biol 4, e377 [CrossRef]
    [Google Scholar]
  65. Rolhion, N., Barnich, N., Claret, L. & Darfeuille-Michaud,A. ( 2005; ). Strong decrease in invasive ability andouter membrane vesicle release in Crohn's disease-associated invasive Escherichia coli strain Lf82 with the yfgL gene deleted. J Bacteriol 187, 2286–2296.[CrossRef]
    [Google Scholar]
  66. Ruiz, N. & Silhavy, T. J. ( 2005; ).Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8, 122–126.[CrossRef]
    [Google Scholar]
  67. Ruiz, N., Falcone, B., Kahn, D. & Silhavy, T. J. ( 2005; ). Chemical conditionality: a genetic strategy to probeorganelle assembly. Cell 121, 307–317.[CrossRef]
    [Google Scholar]
  68. Ruiz, N., Wu, T., Kahne, D. & Silhavy, T. J. ( 2006; ). Probing the barrier function of the outer membrane withchemical conditionality. ACS Chem Biol 1, 385–395.[CrossRef]
    [Google Scholar]
  69. Sankaran, K., Gupta, S. D. & Wu, H. C. ( 1995; ). Modification of bacterial lipoproteins. Methods Enzymol 250, 683–697.
    [Google Scholar]
  70. Schmidt, J. M. & Stanier, R. Y. ( 1966; ). The development of cellular stalks in bacteria. J Cell Biol 28, 423–436.[CrossRef]
    [Google Scholar]
  71. Sciochetti, S. A., Lane, T., Ohta, N. & Newton, A. ( 2002; ). Protein sequences and cellular factors required forpolar localization of a histidine kinase in Caulobacter crescentus. J Bacteriol 184, 6037–6049.[CrossRef]
    [Google Scholar]
  72. Seitz, L. C. & Brun, Y. V. ( 1998; ).Genetic analysis of mecillinam-resistant mutants of Caulobacter crescentus deficient in stalk biosynthesis. J Bacteriol 180, 5235–5239.
    [Google Scholar]
  73. Seydel, A., Gounon, P. & Pugsley, A. P. ( 1999; ). Testing the ‘+2 rule’ for lipoproteinsorting in the Escherichia coli cell envelope with a new geneticselection. Mol Microbiol 34, 810–821.[CrossRef]
    [Google Scholar]
  74. Skerker, J. M. & Shapiro, L. ( 2000; ). Identification and cell-cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 19, 3223–3234.[CrossRef]
    [Google Scholar]
  75. Skerker, J. M., Prasol, M. S., Perchuk, B. S., Biondi, E. G. &Laub, M. T. ( 2005; ). Two-component signal transductionpathways regulating growth and cell cycle progresion in a bacterium: A systems-levelanalysis. PLoS Biol 3, e334 [CrossRef]
    [Google Scholar]
  76. Sklar, J. G., Wu, T., Gronenberg, L. S., Malinverni, J. C.,Kahne, D. & Silhavy, T. J. ( 2007; ). LipoproteinSmpA is a component of the YaeT complex that assembles outer membrane proteinsin Escherichia coli. Proc Natl Acad Sci U S A 104, 6400–6405.[CrossRef]
    [Google Scholar]
  77. Stove, J. L. & Stanier, R. Y. ( 1962; ). Cellular differentiation in stalked bacteria. Nature 196, 1189–1192.[CrossRef]
    [Google Scholar]
  78. Tabb, D. L., McDonald, W. H. & Yates, J. R. ( 2002; ). DTASelect and Contrast: tools for assembling and comparingprotein identifications from shotgun proteomics. J Proteome Res 1, 21–26.[CrossRef]
    [Google Scholar]
  79. Toporowski, M. C., Nomellini, J. F., Awram, P. & Smit, J. ( 2004; ). Two outer membrane proteins are requiredfor maximal type I secretion of the Caulobacter crescentus S-layerprotein. J Bacteriol 186, 8000–8009.[CrossRef]
    [Google Scholar]
  80. Vanini, M. M. T., Spisini, A., Sforca, M. L., Pertinhez, T.A. & Benedetti, C. E. ( 2008; ). The solution structureof the outer membrane lipoprotein OmlA from Xanthomonas axonopodispv. cirtri reveals a protein fold implicated in protein–proteininteraction. Proteins 71, 2051–2064.[CrossRef]
    [Google Scholar]
  81. Viollier, P. H., Sternheim, N. & Shapiro, L. ( 2002; ). A dynamically localized histidine kinase controls the asymmetricdistribution of polar pili proteins. EMBO J 21, 4420–4428.[CrossRef]
    [Google Scholar]
  82. Vogel, J. & Papenfort, K. ( 2006; ).Small non-coding RNAs and the bacterial outer membrane. Curr OpinMicrobiol 9, 605–611.
    [Google Scholar]
  83. Volokhina, E. B., Beckers, F., Tomassen, J. & Bos, M. P. ( 2009; ). The β-barrel outer membraneprotein assembly complex of Neisseria meningitidis. JBacteriol 191, 7074–7085.
    [Google Scholar]
  84. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M. & Tommassen,J. ( 2003; ). Role of a highly conserved bacterial proteinin outer membrane protein assembly. Science 299, 262–265.[CrossRef]
    [Google Scholar]
  85. Vuong, P., Bennion, D., Mantei, J., Frost, D. & Misra, R. ( 2008; ). Analysis of YfgL and YaeT interactions throughbioinformatics, mutagenesis, and biochemistry. J Bacteriol 190, 1507–1517.[CrossRef]
    [Google Scholar]
  86. Wagner, J. K., Galvani, C. D. & Brun, Y. V. ( 2005; ). Caulobacter crescentus requires RodA and MreB forstalk synthesis and prevention of ectopic pole formation. J Bacteriol 187, 544–553.[CrossRef]
    [Google Scholar]
  87. Wagner, J. K., Setayeshgar, S., Sharon, L. A., Reilly, J. P. &Brun, Y. V. ( 2006; ). A nutrient uptake role for bacterialenvelope extensions. Proc Natl Acad Sci U S A 103, 11772–11777.[CrossRef]
    [Google Scholar]
  88. Werner, J. & Misra, R. ( 2005; ). YaeT (Omp85)affects the assembly of lipid-dependent and lipid-independent proteins of Escherichia coli. Mol Microbiol 57, 1450–1459.[CrossRef]
    [Google Scholar]
  89. Wheeler, R. T. & Shapiro, L. ( 1999; ). Differential localization of two histidine kinases controlling bacterialcell differentiation. Mol Cell 4, 683–694.[CrossRef]
    [Google Scholar]
  90. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J. &Kahne, D. ( 2005; ). Identification of a multicomponentcomplex required for outer membrane biogenesis in Escherichia coli. Cell 121, 235–245.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.035055-0
Loading
/content/journal/micro/10.1099/mic.0.035055-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error