Polar localization of Escherichia coli chemoreceptors requires an intact Tol-Pal complex

Molecular Microbiology

Volumn 92, Issue 5, 2014, Pages 985-1004

  Santos, Thiago M A ^a   Lin, Ti Yu ^a   Rajendran, Madhusudan ^a   Anderson, Samantha M ^a   Weibel, Douglas B ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Wisconsin Madison   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; MULTIPROTEIN COMPLEX; TOL PAL COMPLEX; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN;

ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIUM MUTANT; CELL DIVISION; CELL MOTILITY; CELL POLARITY; CELLULAR DISTRIBUTION; CHEMORECEPTOR; CHEMOTAXIS; CONTROLLED STUDY; ESCHERICHIA COLI; LIPID COMPOSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REGULATORY MECHANISM; METABOLISM;

BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS;

EID: 84901402304     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12609     Document Type: Article

References (124)

1. Alley, M.R., Maddock, J.R., and Shapiro, L. (1992) Polar localization of a bacterial chemoreceptor. Genes Dev 6: 825-836.
2. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
3. Bernadac, A., Gavioli, M., Lazzaroni, J.-C., Raina, S., and Lloubès, R. (1998) Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180: 4872-4878.
4. Bouveret, E., Derouiche, R., Rigal, A., Lloubès, R., Lazdunski, C., and Bénédetti, H. (1995) Peptidoglycan-associated lipoprotein-TolB interaction. A possible key to explaining the formation of contact sites between the inner and outer membranes of Escherichia coli. J Biol Chem 270: 11071-11077.
5. Bouveret, E., Bénédetti, H., Rigal, A., Loret, E., and Lazdunski, C. (1999) In vitro characterization of peptidoglycan-associated lipoprotein (PAL) - peptidoglycan and PAL-TolB interactions. J Bacteriol 181: 6306-6311.
6. Bowman, G.R., Comolli, L.R., Zhu, J., Eckart, M., Koenig, M., Downing, K.H., etal. (2008) A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134: 945-955.
7. Braun, V. (1975) Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim Biophys Acta 415: 335-377.
8. Braun, V. (1995) Energy-coupled transport and signal transduction through the gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol Rev 16: 295-307.
9. Bray, D., Levin, M.D., and Morton-Firth, C.J. (1998) Receptor clustering as a cellular mechanism to control sensitivity. Nature 393: 85-88.
10. Briegel, A., Ding, H.J., Li, Z., Werner, J., Gitai, Z., Dias, D.P., etal. (2008) Location and architecture of the Caulobacter crescentus chemoreceptor array. Mol Microbiol 69: 30-41.
11. Briegel, A., Ortega, D.R., Tocheva, E.I., Wuichet, K., Li, Z., Chen, S., etal. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106: 17181-17186.
12. Briegel, A., Li, X., Bilwes, A.M., Hughes, K.T., Jensen, G.J., and Crane, B.R. (2012) Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. Proc Natl Acad Sci USA 109: 3766-3771.
13. Cascales, E., Lloubès, R., and Sturgis, J.N. (2001) The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42: 795-807.
14. Charles, M., Pérez, M., Kobil, J.H., and Goldberg, M.B. (2001) Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. Proc Natl Acad Sci USA 98: 9871-9876.
15. Chiu, S.-W., Roberts, M.A.J., Leake, M.C., and Armitage, J.P. (2013) Positioning of chemosensory proteins and FtsZ through the Rhodobacter sphaeroides cell cycle. Mol Microbiol 90: 322-337.
16. Choi, D.S., Yamada, H., Mizuno, T., and Mizushima, S. (1986) Trimeric structure and localization of the major lipoprotein in the cell surface of Escherichia coli. J Biol Chem 261: 8953-8957.
17. Chung, C.T., Niemela, S.L., and Miller, R.H. (1989) One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci USA 86: 2172-2175.
18. Clavel, T., Germon, P., Vianney, A., Portalier, R., and Lazzaroni, J.-C. (1998) TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29: 359-367.
19. Click, E., and Webster, R. (1997) Filamentous phage infection: required interactions with the TolA protein. J Bacteriol 179: 6464-6471.
20. Copeland, M.F., Flickinger, S.T., Tuson, H.H., and Weibel, D.B. (2010) Studying the dynamics of flagella in multicellular communities of Escherichia coli by using biarsenical dyes. Appl Environ Microbiol 76: 1241-1250.
21. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
22. Davies, J.K., and Reeves, P. (1975) Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. J Bacteriol 123: 102-117.
23. Derouiche, R., Bénédetti, H., Lazzaroni, J.-C., Lazdunski, C., and Lloubès, R. (1995) Protein complex within Escherichia coli inner membrane. TolA N-terminal domain interacts with TolQ and TolR proteins. J Biol Chem 270: 11078-11084.
24. Derouiche, R., Gavioli, M., Bénédetti, H., Prilipov, A., Lazdunski, C., and Lloubès, R. (1996) TolA central domain interacts with Escherichia coli porins. EMBO J 15: 6408-6415.
25. Dubuisson, J.F., Vianney, A., and Lazzaroni, J.-C. (2002) Mutational analysis of the TolA C-terminal domain of Escherichia coli and genetic evidence for an interaction between TolA and TolB. J Bacteriol 184: 4620-4625.
26. Ebersbach, G., Briegel, A., Jensen, G.J., and Jacobs-Wagner, C. (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134: 956-968.
27. Englert, D.L., Jayaraman, A., and Manson, M.D. (2009) Microfluidic techniques for the analysis of bacterial chemotaxis. Methods Mol Biol 571: 1-23.
28. Gan, L., Chen, S., and Jensen, G.J. (2008) Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci USA 105: 18953-18957.
29. Gaspar, J.A., Thomas, J.A., Marolda, C.L., and Valvano, M.A. (2000) Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the function of the TolA protein. Mol Microbiol 38: 262-275.
30. Gerding, M.A., Ogata, Y., Pecora, N.D., Niki, H., and de Boer, P.A. (2007) The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol Microbiol 63: 1008-1025.
31. Germon, P., Clavel, T., Vianney, A., Portalier, R., and Lazzaroni, J.-C. (1998) Mutational analysis of the Escherichia coli K-12 TolA N-terminal region and characterization of its TolQ-interacting domain by genetic suppression. J Bacteriol 180: 6433-6439.
32. Gestwicki, J.E., and Kiessling, L.L. (2002) Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415: 81-84.
33. Gestwicki, J.E., Lamanna, A.C., Harshey, R.M., McCarter, L.L., Kiessling, L.L., and Adler, J. (2000) Evolutionary conservation of methyl-accepting chemotaxis protein location in Bacteria and Archaea. J Bacteriol 182: 6499-6502.
34. Gold, V.A.M., Robson, A., Bao, H., Romantsov, T., Duong, F., and Collinson, I. (2010) The action of cardiolipin on the bacterial translocon. Proc Natl Acad Sci USA 107: 10044-10049.
35. Goldberg, M.B., Bârzu, O., Parsot, C., and Sansonetti, P.J. (1993) Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol 175: 2189-2196.
36. Greenfield, D., McEvoy, A.L., Shroff, H., Crooks, G.E., Wingreen, N.S., Betzig, E., etal. (2009) Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 7: e1000137.
37. Hazelbauer, G.L., Falke, J.J., and Parkinson, J.S. (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9-19.
38. Hendrick, J.P., and Wickner, W. (1991) SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J Biol Chem 266: 24596-24600.
39. Huang, K.C., and Ramamurthi, K.S. (2010) Macromolecules that prefer their membranes curvy. Mol Microbiol 76: 822-832.
40. Huang, K.C., Mukhopadhyay, R., and Wingreen, N.S. (2006) A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput Biol 2: e151.
41. Inouye, M., Shaw, J., and Shen, C. (1972) The assembly of a structural lipoprotein in the envelope of Escherichia coli. J Biol Chem 247: 8154-8159.
42. Isnard, M., Rigal, A., Lazzaroni, J.-C., Lazdunski, C., and Lloubès, R. (1994) Maturation and localization of the TolB protein required for colicin import. J Bacteriol 176: 6392-6396.
43. Janakiraman, A., Fixen, K.R., Gray, A.N., Niki, H., and Goldberg, M.B. (2009) A genome-scale proteomic screen identifies a role for DnaK in chaperoning of polar autotransporters in Shigella. J Bacteriol 191: 6300-6311.
44. Kampfenkel, K., and Braun, V. (1993) Membrane topologies of the TolQ and TolR proteins of Escherichia coli: inactivation of TolQ by a missense mutation in the proposed first transmembrane segment. J Bacteriol 175: 4485-4491.
45. Kentner, D., Thiem, S., Hildenbeutel, M., and Sourjik, V. (2006) Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61: 407-417.
46. Kikuchi, S., Shibuya, I., and Matsumoto, K. (2000) Viability of an Escherichia coli pgsA null mutant lacking detectable phosphatidylglycerol and cardiolipin. J Bacteriol 182: 371-376.
47. Kitagawa, M., Ara, T., Arifuzzaman, M., Ioka-Nakamichi, T., Inamoto, E., Toyonaga, H., etal. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12: 291-299.
48. Kitchen, J.L., Li, Z., and Crooke, E. (1999) Electrostatic interactions during acidic phospholipid reactivation of DnaA protein, the Escherichia coli initiator of chromosomal replication. Biochemistry 38: 6213-6221.
49. Koebnik, R. (1995) Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol Microbiol 16: 1269-1270.
50. Koppelman, C.M., Den Blaauwen, T., Duursma, M.C., Heeren, R.M., and Nanninga, N. (2001) Escherichia coli minicell membranes are enriched in cardiolipin. J Bacteriol 183: 6144-6147.
51. Lahiri, A., Ananthalakshmi, T.K., Nagarajan, A.G., Ray, S., and Chakravortty, D. (2011) TolA mediates the differential detergent resistance pattern between the Salmonella enterica subsp. enterica serovars Typhi and Typhimurium. Microbiology 157: 1402-1415.
52. Lai, E.-M., Nair, U., Phadke, N.D., and Maddock, J.R. (2004) Proteomic screening and identification of differentially distributed membrane proteins in Escherichia coli. Mol Microbiol 52: 1029-1044.
53. Laloux, G., and Jacobs-Wagner, C. (2014) How do bacteria localize proteins to the cell pole? J Cell Sci 127: 11-19.
54. Lam, H., Schofield, W.B., and Jacobs-Wagner, C. (2006) A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124: 1011-1023.
55. Lazzaroni, J.-C., and Portalier, R. (1992) The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (PAL). Mol Microbiol 6: 735-742.
56. Lazzaroni, J.-C., Vianney, A., Popot, J.L., Bénédetti, H., Samatey, F., Lazdunski, C., etal. (1995) Transmembrane alpha-helix interactions are required for the functional assembly of the Escherichia coli Tol complex. J Mol Biol 246: 1-7.
57. Lazzaroni, J.-C., Germon, P., Ray, M.-C., and Vianney, A. (1999) The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177: 191-197.
58. Lazzaroni, J.-C., Dubuisson, J.-F., and Vianney, A. (2002) The Tol proteins of Escherichia coli and their involvement in the translocation of group A colicins. Biochimie 84: 391-397.
59. Lenarcic, R., Halbedel, S., Visser, L., Shaw, M., Wu, L.J., Errington, J., etal. (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28: 2272-2282.
60. Levengood, S.K., Beyer, W.F., and Webster, R.E. (1991) TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc Natl Acad Sci USA 88: 5939-5943.
61. Li, G., and Young, K.D. (2012) Isolation and identification of new inner membrane-associated proteins that localize to cell poles in Escherichia coli. Mol Microbiol 84: 276-295.
62. Lill, R., Dowhan, W., and 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: 271-280.
63. Liu, J., Hu, B., Morado, D.R., Jani, S., Manson, M.D., and Margolin, W. (2012) Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells. Proc Natl Acad Sci USA 109: E1481-E1488.
64. Llamas, M.A., Ramos, J.L., and Rodríguez-Herva, J.J. (2000) Mutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J Bacteriol 182: 4764-4772.
65. Llamas, M.A., Rodríguez-Herva, J.J., Hancock, R.E.W., Bitter, W., Tommassen, J., and Ramos, J.L. (2003) Role of Pseudomonas putida tol-oprL gene products in uptake of solutes through the cytoplasmic membrane. J Bacteriol 185: 4707-4716.
66. Lloubès, R., Cascales, E., Walburger, A., Bouveret, E., Lazdunski, C., Bernadac, A., etal. (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152: 523-529.
67. Lybarger, S.R., and Maddock, J.R. (2001) Polarity in action: asymmetric protein localization in bacteria. J Bacteriol 183: 3261-3267.
68. Maddock, J.R., and Shapiro, L. (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717-1723.
69. Marston, A.L., and Errington, J. (1999) Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell 4: 673-682.
70. Matsumoto, K. (2001) Dispensable nature of phosphatidylglycerol in Escherichia coli: dual roles of anionic phospholipids. Mol Microbiol 39: 1427-1433.
71. Mileykovskaya, E., and 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: 1172-1175.
72. Mileykovskaya, E., Fishov, I., Fu, X., Corbin, B.D., Margolin, W., and Dowhan, W. (2003) Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 278: 22193-22198.
73. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
74. Miller, L.D., Russell, M.H., and Alexandre, G. (2009) Diversity in bacterial chemotactic responses and niche adaptation. Adv Appl Microbiol 66: 53-75.
75. Mizushima, T., Koyanagi, R., Suzuki, E., Tomura, A., Kutsukake, K., Miki, T., and Sekimizu, K. (1995) Control by phosphatidylglycerol of expression of the flhD gene in Escherichia coli. Biochim Biophys Acta 1245: 397-401.
76. Morgan, D.G., Baumgartner, J.W., and Hazelbauer, G.L. (1993) Proteins antigenically related to methyl-accepting chemotaxis proteins of Escherichia coli detected in a wide range of bacterial species. J Bacteriol 175: 133-140.
77. Muller, M.M., and Webster, R.E. (1997) Characterization of the tol-pal and cyd region of Escherichia coli K-12: transcript analysis and identification of two new proteins encoded by the cyd operon. J Bacteriol 179: 2077-2080.
78. Muller, M.M., Vianney, A., Lazzaroni, J.-C., Webster, R.E., and Portalier, R. (1993) Membrane topology of the Escherichia coli TolR protein required for cell envelope integrity. J Bacteriol 175: 6059-6061.
79. Okuda, S., Freinkman, E., and Kahne, D. (2012) Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338: 1214-1217.
80. Porter, S.L., Wadhams, G.H., and Armitage, J.P. (2011) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9: 153-165.
81. Ramamurthi, K.S., and Losick, R. (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci USA 106: 13541-13545.
82. Ramamurthi, K.S., Lecuyer, S., Stone, H.A., and Losick, R. (2009) Geometric cue for protein localization in a bacterium. Science 323: 1354-1357.
83. Ray, M.C., Germon, P., Vianney, A., Portalier, R., and Lazzaroni, J.-C. (2000) Identification by genetic suppression of Escherichia coli TolB residues important for TolB-Pal interaction. J Bacteriol 182: 821-824.
84. Renner, L.D., and Weibel, D.B. (2011) Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes. Proc Natl Acad Sci USA 2011: 6264-6269.
85. Renner, L.D., and Weibel, D.B. (2012) MinD and MinE interact with anionic phospholipids and regulate division plane formation in Escherichia coli. J Biol Chem 287: 38835-38844.
86. Renner, L.D., Eswaramoorthy, P., Ramamurthi, K.S., and Weibel, D.B. (2013) Studying biomolecular localization by engineering bacterial cell wall curvature. PLoS ONE 8: e84143.
87. Rigal, A., Bouveret, E., Lloubès, R., Lazdunski, C., and Bénédetti, H. (1997) The TolB protein interacts with the porins of Escherichia coli. J Bacteriol 179: 7274-7279.
88. Ringgaard, S., Schirner, K., Davis, B.M., and Waldor, M.K. (2011) A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins. Genes Dev 25: 1544-1555.
89. Romantsov, T., Helbig, S., Culham, D.E., Gill, C., Stalker, L., and Wood, J.M. (2007) Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli. Mol Microbiol 64: 1455-1465.
90. Romantsov, T., Stalker, L., Culham, D.E., and Wood, J.M. (2008) Cardiolipin controls the osmotic stress response and the subcellular location of transporter ProP in Escherichia coli. J Biol Chem 283: 12314-12323.
91. Romantsov, T., Battle, A.R., Hendel, J.L., Martinac, B., and Wood, J.M. (2010) Protein localization in Escherichia coli cells: comparison of the cytoplasmic membrane proteins ProP, LacY, ProW, AqpZ, MscS, and MscL. J Bacteriol 192: 912-924.
92. Rudner, D.Z., and Losick, R. (2010) Protein subcellular localization in bacteria. Cold Spring Harb Perspect Biol 2: a000307.
93. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
94. Shapiro, L., McAdams, H.H., and Losick, R. (2002) Generating and exploiting polarity in bacteria. Science 298: 1942-1946.
95. Shiba, Y., Yokoyama, Y., Aono, Y., Kiuchi, T., Kusaka, J., Matsumoto, K., etal. (2004) Activation of the Rcs signal transduction system is responsible for the thermosensitive growth defect of an Escherichia coli mutant lacking phosphatidylglycerol and cardiolipin. J Bacteriol 186: 6526-6535.
96. Shimizu, T.S., Le Novére, N., Levin, M.D., Beavil, A.J., Sutton, B.J., and Bray, D. (2000) Molecular model of a lattice of signalling proteins involved in bacterial chemotaxis. Nat Cell Biol 2: 792-796.
97. Shiomi, D., Zhulin, I.B., Homma, M., and Kawagishi, I. (2002) Dual recognition of the bacterial chemoreceptor by chemotaxis-specific domains of the CheR methyltransferase. J Biol Chem 277: 42325-42333.
98. Shiomi, D., Yoshimoto, M., Homma, M., and Kawagishi, I. (2006) Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol Microbiol 60: 894-906.
99. Shu, W., Liu, J., Ji, H., and Lu, M. (2000) Core structure of the outer membrane lipoprotein from Escherichia coli at 1.9 Å resolution. J Mol Biol 299: 1101-1112.
100. Skareso, J.T., Ahmern, B.M.M., Seachordll, C.L., Darveau, R.P., and Postle, K. (1993) Energy transduction between membranes. J Biol Chem 268: 16302-16308.
101. Skidmore, J.M., Ellefson, D.D., McNamara, B.P., Couto, M.M., Wolfe, A.J., and Maddock, J.R. (2000) Polar clustering of the chemoreceptor complex in Escherichia coli occurs in the absence of complete CheA function. J Bacteriol 182: 967-973.
102. Sliusarenko, O., Heinritz, J., Emonet, T., and Jacobs-Wagner, C. (2011) High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80: 612-627.
103. Sourjik, V., and Armitage, J.P. (2010) Spatial organization in bacterial chemotaxis. EMBO J 29: 2724-2733.
104. Sourjik, V., and Berg, H. (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99: 123-127.
105. Steinhauer, J., Agha, R., Pham, T., Varga, A.W., and Goldberg, M.B. (1999) The unipolar Shigella surface protein IcsA is targeted directly to the bacterial old pole: IcsP cleavage of IcsA occurs over the entire bacterial surface. Mol Microbiol 32: 367-377.
106. Sturgis, J.N. (2001) Organisation and evolution of the tol-pal gene cluster. J Mol Microbiol Biotechnol 3: 113-122.
107. Tan, B.K., Bogdanov, M., Zhao, J., Dowhan, W., Raetz, C.R.H., and Guan, Z. (2012) Discovery of a cardiolipin synthase utilizing phosphatidylethanolamine and phosphatidylglycerol as substrates. Proc Natl Acad Sci USA 109: 16504-16509.
108. Thiem, S., and Sourjik, V. (2008) Stochastic assembly of chemoreceptor clusters in Escherichia coli. Mol Microbiol 68: 1228-1236.
109. Thiem, S., Kentner, D., and Sourjik, V. (2007) Positioning of chemosensory clusters in E. coli and its relation to cell division. EMBO J 26: 1615-1623.
110. Tomura, A., Ishikawa, T., Sagara, Y., Miki, T., and Sekimizu, K. (1993) Requirement of phosphatidylglycerol for flagellation of Escherichia coli. FEBS Lett 329: 287-290.
111. Turner, L., Ryu, W.S., and Berg, H.C. (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182: 2793-2801.
112. Tuson, H.H., Copeland, M.F., Carey, S., Sacotte, R., and Weibel, D.B. (2013) Flagellum density regulates Proteus mirabilis swarmer cell motility in viscous environments. J Bacteriol 195: 368-377.
113. Vianney, A., Lewin, T.M., Beyer, W.F., Lazzaroni, J.-C., Portalier, R., and Webster, R.E. (1994) Membrane topology and mutational analysis of the TolQ protein of Escherichia coli required for the uptake of macromolecules and cell envelope integrity. J Bacteriol 176: 822-829.
114. Vianney, A., Muller, M.M., Clavel, T., Lazzaroni, J.-C., Portalier, R., and Webster, R.E. (1996) Characterization of the tol-pal region of Escherichia coli K-12: translational control of tolR expression by TolQ and identification of a new open reading frame downstream of pal encoding a periplasmic protein. J Bacteriol 178: 4031-4038.
115. de Vrije, T., de Swart, R.L., Dowhan, W., Tommassen, J., and de Kruijff, B. (1988) Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature 334: 173-175.
116. Wadhams, G.H., and Armitage, J.P. (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5: 1024-1037.
117. Walburger, A., Lazdunski, C., and Corda, Y. (2002) The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. Mol Microbiol 44: 695-708.
118. Wang, H., Wingreen, N., and Mukhopadhyay, R. (2008) Self-Organized periodicity of protein clusters in growing bacteria. Phys Rev Lett 101: 218101.
119. Werner, J.N., Chen, E.Y., Guberman, J.M., Zippilli, A.R., Irgon, J.J., and Gitai, Z. (2009) Quantitative genome-scale analysis of protein localization in an asymmetric bacterium. Proc Natl Acad Sci USA 106: 7858-7863.
120. Wu, J., Li, J., Li, G., Long, D.G., and Weis, R.M. (1996) The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation. Biochemistry 35: 4984-4993.
121. Yamaichi, Y., Bruckner, R., Ringgaard, S., Moll, A., Cameron, D.E., Briegel, A., etal. (2012) A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev 26: 2348-2360.
122. Yeh, Y.-C., Comolli, L.R., Downing, K.H., Shapiro, L., and McAdams, H.H. (2010) The Caulobacter Tol-Pal complex is essential for outer membrane integrity and the positioning of a polar localization factor. J Bacteriol 192: 4847-4858.
123. Zhang, P., Khursigara, C.M., Hartnell, L.M., and Subramaniam, S. (2007) Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc Natl Acad Sci USA 104: 3777-3781.
124. Zhou, Q., Ames, P., and Parkinson, J.S. (2011) Biphasic control logic of HAMP domain signalling in the Escherichia coli serine chemoreceptor. Mol Microbiol 80: 596-611.