Supramolecular assemblies underpin turnover of outer membrane proteins in bacteria

Nature

Volumn 523, Issue 7560, 2015, Pages 333-336

  Rassam, Patrice ^a,b   Copeland, Nikki A ^b,d   Birkholz, Oliver ^c   Tóth, Csaba ^b,e   Chavent, Matthieu ^a   Duncan, Anna L ^a   Cross, Stephen J ^b,f   Housden, Nicholas G ^a   Kaminska, Renata ^a   Seger, Urban ^b,g   Quinn, Diana M ^b   Garrod, Tamsin J ^b,h   Sansom, Mark S P ^a   Piehler, Jacob ^c   Baumann, Christoph G ^b   Kleanthous, Colin ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF OSNABRÜCK   (Germany)

^d LANCASTER UNIVERSITY   (United Kingdom)

^e GSK Slovakia sro   (Slovakia)

^f UNIVERSITY OF BRISTOL   (United Kingdom)

^g Biomedizinische Analytik HF Max Daetwyler Platz 2   (Switzerland)

^h UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; BAMA PROTEIN, E COLI; BAMC PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; LIPID LINKED PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN BINDING;

CELL ORGANELLE; COLIFORM BACTERIUM; FLUORESCENCE; HABITAT TYPE; MEMBRANE; MOLECULAR ANALYSIS; PROTEIN; RIVER WATER; TURNOVER;

ARTICLE; BIOGENESIS; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; OUTER MEMBRANE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SUPRAMOLECULAR CHEMISTRY; TURNOVER TIME; CELL POLARITY; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; DIFFUSION; GENETICS; METABOLISM; PROTEIN TRANSPORT;

ANIMALIA; ESCHERICHIA COLI; NEGIBACTERIA;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL POLARITY; DIFFUSION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPID-LINKED PROTEINS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MOLECULAR DYNAMICS SIMULATION; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84937422188     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14461     Document Type: Article

References (58)

1. van Elsas, J.D., Semenov, A. V., Costa, R. & Trevors, J. T. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J. 5, 173-183 (2011).
2. Tenaillon, O., Skurnik, D., Picard, B. & Denamur, E. The population genetics of commensal Escherichia coli. Nature Rev. Microbiol. 8, 207-217 (2010).
3. Morabito, S. (ed.) Pathogenic Escherichia coli: Molecular & cellular microbiology (Caister Academic Press, 2014).
4. Vogel, J. & Papenfort, K. Small non-coding RNAs and the bacterial outer membrane. Curr. Opin. Microbiol. 9, 605-611 (2006).
5. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656 (2003).
6. Moon, C. P., Zaccai, N. R., Fleming, P. J., Gessmann, D. & Fleming, K. G. Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm. Proc. Natl Acad. Sci. USA 110, 4285-4290 (2013).
7. Hagan, C. L., Silhavy, T. J. & Kahne, D. b-Barrelmembrane protein assembly by the Bam complex. Annu. Rev. Biochem. 80, 189-210 (2011).
8. Noinaj, N. et al. Structural insight into the biogenesis of b-barrel membrane proteins. Nature 501, 385-390 (2013).
9. Kleanthous, C. Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nature Rev. Microbiol. 8, 843-848 (2010).
10. Housden, N. G. et al. Intrinsically disordered protein threads through the bacterial outer membrane porin OmpF. Science 340, 1570-1574 (2013).
11. Shapiro, L., McAdams, H. H. & Losick, R. Why and how bacteria localize proteins. Science 326, 1225-1228 (2009).
12. Housden, N. G., Loftus, S. R., Moore, G. R., James, R. & Kleanthous, C. Cell entry mechanism of enzymatic bacterial colicins: porin recruitment and the thermodynamics of receptor binding. Proc. Natl Acad. Sci. USA 102, 13849-13854 (2005).
13. Kurisu, G. et al. The structure of BtuB with bound colicin E3 R-domain implies a translocon. Nature Struct. Biol. 10, 948-954 (2003).
14. Buchanan, S. K. et al. Structure of colicin I receptor bound to the R-domain of colicin Ia: implications for protein import. EMBO J. 26, 2594-2604 (2007).
15. Mullineaux, C. W., Nenninger, A., Ray, N. & Robinson, C. Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J. Bacteriol. 188, 3442-3448 (2006).
16. Verhoeven, G.S., Dogterom, M. & den Blaauwen, T. Absence of long-range diffusion of OmpA in E. coli is not caused by its peptidoglycan binding domain. BMC Microbiol. 13, 66 (2013).
17. Smit, J. & Nikaido, H. Outer membrane of Gram-negative bacteria. XVIII. Electron microscopic studies on porin insertion sites and growth of cell surface of Salmonella typhimurium. J. Bacteriol. 135, 687-702 (1978).
18. Ursell, T. S., Trepagnier, E. H., Huang, K.C. & Theriot, J. A. Analysis of surface protein expression reveals the growth pattern of the Gram-negative outer membrane. PLOS Comput. Biol. 8, e1002680 (2012).
19. Browning, D. F. et al. Mutational and topological analysis of the Escherichia coli BamA protein. PLoS ONE 8, e84512 (2013).
20. Webb, C. T. et al. Dynamic association of BAM complexmodules includes surface exposure of the lipoprotein BamC. J. Mol. Biol. 422, 545-555 (2012).
21. Roder, F. et al. Reconstitution of membrane proteins into polymer-supported membranes for probing diffusion and interactions by singlemolecule techniques. Anal. Chem. 83, 6792-6799 (2011).
22. White, J. C., DiGirolamo, P. M., Fu, M. L., Preston, Y. A. & Bradbeer, C. Transport of vitamin B12 in Escherichia coli. Location and properties of the initial B12-binding site. J. Biol. Chem. 248, 3978-3986 (1973).
23. Casuso, I. et al. Characterization of the motion of membrane proteins using highspeed atomic force microscopy. Nature Nanotechnol. 7, 525-529 (2012).
24. Goose, J. E. & Sansom, M. S. Reduced lateral mobility of lipids and proteins in crowded membranes. PLOS Comput. Biol. 9, e1003033 (2013).
25. Jarosławski, S., Duquesne, K., Sturgis, J. N. & Scheuring, S. High-resolution architecture of the outer membrane of the Gram-negative bacteria Roseobacter denitrificans. Mol. Microbiol. 74, 1211-1222 (2009).
26. Stewart, E. J., Madden, R., Paul, G. & Taddei, F. Aging and death in an organismthat reproduces by morphologically symmetric division. PLoS Biol. 3, e45 (2005).
27. Laloux, G. & Jacobs-Wagner, C. Howdo bacteria localize proteins to the cell pole? J. Cell Sci. 127, 11-19 (2014).
28. Qiao, S., Luo, Q., Zhao, Y., Zhang, X. C. & Huang, Y. Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 511, 108-111 (2014).
29. Ieva, R., Tian, P., Peterson, J. H. & Bernstein, H. D. Sequential and spatially restricted interactions of assembly factors with an autotransporter β domain. Proc. Natl Acad. Sci. USA 108, E383-E391 (2011).
30. Konovalova, A., Perlman, D. H., Cowles, C. E. & Silhavy, T. J. Transmembrane domain of surface-exposed outermembrane lipoprotein RcsF is threaded through the lumen of β-barrel proteins. Proc. Natl Acad. Sci. USA 111, E4350-E4358 (2014).
31. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006).
32. Penfold, C. N. et al. Flexibility in the receptor-binding domain of the enzymatic colicin E9 is required for toxicity against Escherichia coli cells. J. Bacteriol. 186, 4520-4527 (2004).
33. Garinot-Schneider, C., Pommer, A. J., Moore, G. R., Kleanthous, C. & James, R. Identification of putative active-site residues in the DNase domain of colicin E9 by random mutagenesis. J. Mol. Biol. 260, 731-742 (1996).
34. Roder, F., Birkholz, O., Beutel, O., Paterok, D. & Piehler, J. Spatial organization of lipid phases in micropatterned polymer-supportedmembranes. J. Am. Chem. Soc. 135, 1189-1192 (2013).
35. Yin, J. et al. Genetically encoded short peptide tag for versatile protein labeling by Sfp phosphopantetheinyl transferase. Proc. Natl Acad. Sci. USA 102, 15815-15820 (2005).
36. Ray, N., Nenninger, A., Mullineaux, C. W. & Robinson, C. Location and mobility of twin arginine translocase subunits in the Escherichia coli plasma membrane. J. Biol. Chem. 280, 17961-17968 (2005).
37. Mashanov, G. I. & Molloy, J. E. Automatic detection of single fluorophores in live cells. Biophys. J. 92, 2199-2211 (2007).
38. Kusumi, A., Sako, Y. & Yamamoto, M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 65, 2021-2040 (1993).
39. Deich, J., Judd, E. M., McAdams, H. H. & Moerner, W. E. Visualization of the movement of single histidine kinasemolecules in live Caulobacter cells. Proc. Natl Acad. Sci. USA 101, 15921-15926 (2004).
40. Leake, M. C. et al. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443, 355-358 (2006).
41. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675 (2012).
42. Zinchuk, V., Wu, Y., Grossenbacher-Zinchuk, O. & Stefani, E. Quantifying spatial correlations of fluorescent markers using enhanced background reduction with protein proximity index and correlation coefficient estimations. Nature Protocols 6, 1554-1567 (2011).
43. Degrip, W. J., Vanoostrum, J. & Bovee-Geurts, P. H. Selective detergent-extraction from mixed detergent/lipid/protein micelles, using cyclodextrin inclusion compounds: a novel generic approach for the preparation of proteoliposomes. Biochem. J. 330, 667-674 (1998).
44. Vogelsang, J. et al. A reducing and oxidizing system minimizes photobleaching and blinking of fluorescent dyes. Angew. Chem. 47, 5465-5469 (2008).
45. Espenel, C. et al. Single-molecule analysis of CD9 dynamics and partitioning reveals multiple modes of interaction in the tetraspanin web. J. Cell Biol. 182, 765-776 (2008).
46. Krementsov, D. N. et al. HIV-1 assembly differentially alters dynamics and partitioning of tetraspanins and raft components. Traffic 11, 1401-1414 (2010).
47. Marrink, S. J., Risselada, H. J., Yefimov, S., Tieleman, D. P. & de Vries, A. H. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B 111, 7812-7824 (2007).
48. Bond, P. J., Wee, C. L. & Sansom, M. S. Coarse-grained molecular dynamics simulations of the energetics of helix insertion into a lipid bilayer. Biochemistry 47, 11321-11331 (2008).
49. Bond, P. J. & Sansom, M. S. Insertion and assembly of membrane proteins via simulation. J. Am. Chem. Soc. 128, 2697-2704 (2006).
50. Klauda, J. B., Brooks, B. R. & Pastor, R.W. Dynamical motions of lipids and a finite size effect in simulations of bilayers. J. Chem. Phys. 125, 144710 (2006).
51. Michaud-Agrawal, N., Denning, E. J., Woolf, T. B. & Beckstein, O. MDAnalysis: A toolkit for the analysis ofmolecular dynamics simulations. J. Comput. Chem., (2011).
52. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996).
53. Jones, S. & Thornton, J. M. Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA 93, 13-20 (1996).
54. Javanainen, M. et al. Anomalous and normal diffusion of proteins and lipids in crowded lipid membranes. Faraday Disc. 161, 397-417 (2013).
55. Oddershede, L., Dreyer, J. K., Grego, S., Brown, S. & Berg-Sorensen, K. Themotion of a singlemolecule, the lambda-receptor, in the bacterial outermembrane. Biophys. J. 83, 3152-3161 (2002).
56. Spector, J. et al. Mobility of BtuBandOmpF in the Escherichia colioutermembrane: implications for dynamic formation of a translocon complex. Biophys. J. 99, 3880-3886 (2010).
57. Leake, M. C. et al. Variable stoichiometry of the TatA component of the twinarginine protein transport system observed by in vivo single-molecule imaging. Proc. Natl Acad. Sci. USA 105, 15376-15381 (2008).
58. Jeanteur, D. et al. Structural and functional alterations of a colicin-resistantmutant of OmpF porin from Escherichia coli. Proc. Natl Acad. Sci. USA 91, 10675-10679 (1994).