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Cryo-EM structures reveal multiple stages of bacterial outer membrane protein folding.

Doyle MT, Jimah JR, Dowdy T, Ohlemacher SI, Larion M, Hinshaw JE, Bernstein HD
Cell 185 1143-1156.e13 (2022)
Related entries: 7tsz, 7tt0, 7tt1, 7tt2, 7tt4, 7tt5, 7tt6, 7tt7, 7ttc

Cited: 18 times
EuropePMC logo PMID: 35294859

Abstract

Transmembrane β barrel proteins are folded into the outer membrane (OM) of Gram-negative bacteria by the β barrel assembly machinery (BAM) via a poorly understood process that occurs without known external energy sources. Here, we used single-particle cryo-EM to visualize the folding dynamics of a model β barrel protein (EspP) by BAM. We found that BAM binds the highly conserved "β signal" motif of EspP to correctly orient β strands in the OM during folding. We also found that the folding of EspP proceeds via "hybrid-barrel" intermediates in which membrane integrated β sheets are attached to the essential BAM subunit, BamA. The structures show an unprecedented deflection of the membrane surrounding the EspP intermediates and suggest that β sheets progressively fold toward BamA to form a β barrel. Along with in vivo experiments that tracked β barrel folding while the OM tension was modified, our results support a model in which BAM harnesses OM elasticity to accelerate β barrel folding.

Articles - 7tt3 mentioned but not cited (1)

  1. Cryo-EM structures reveal multiple stages of bacterial outer membrane protein folding. Doyle MT, Jimah JR, Dowdy T, Ohlemacher SI, Larion M, Hinshaw JE, Bernstein HD. Cell 185 1143-1156.e13 (2022)


Reviews citing this publication (3)

  1. Detergent-Free Isolation of Membrane Proteins and Strategies to Study Them in a Near-Native Membrane Environment. Krishnarjuna B, Ramamoorthy A. Biomolecules 12 1076 (2022)
  2. Surveying membrane landscapes: a new look at the bacterial cell surface. Lithgow T, Stubenrauch CJ, Stumpf MPH. Nat Rev Microbiol (2023)
  3. Visualizing Intramolecular Dynamics of Membrane Proteins. Ohkubo T, Shiina T, Kawaguchi K, Sasaki D, Inamasu R, Yang Y, Li Z, Taninaka K, Sakaguchi M, Fujimura S, Sekiguchi H, Kuramochi M, Arai T, Tsuda S, Sasaki YC, Mio K. Int J Mol Sci 23 14539 (2022)

Articles citing this publication (14)

  1. Lipids mediate supramolecular outer membrane protein assembly in bacteria. Webby MN, Oluwole AO, Pedebos C, Inns PG, Olerinyova A, Prakaash D, Housden NG, Benn G, Sun D, Hoogenboom BW, Kukura P, Mohammed S, Robinson CV, Khalid S, Kleanthous C. Sci Adv 8 eadc9566 (2022)
  2. Small Molecule Antibiotics Inhibit Distinct Stages of Bacterial Outer Membrane Protein Assembly. Peterson JH, Doyle MT, Bernstein HD. mBio 13 e0228622 (2022)
  3. Peptidoglycan maturation controls outer membrane protein assembly. Mamou G, Corona F, Cohen-Khait R, Housden NG, Yeung V, Sun D, Sridhar P, Pazos M, Knowles TJ, Kleanthous C, Vollmer W. Nature 606 953-959 (2022)
  4. A multipoint guidance mechanism for β-barrel folding on the SAM complex. Takeda H, Busto JV, Lindau C, Tsutsumi A, Tomii K, Imai K, Yamamori Y, Hirokawa T, Motono C, Ganesan I, Wenz LS, Becker T, Kikkawa M, Pfanner N, Wiedemann N, Endo T. Nat Struct Mol Biol 30 176-187 (2023)
  5. BamE directly interacts with BamA and BamD coordinating their functions. Kumar S, Konovalova A. Mol Microbiol 120 397-407 (2023)
  6. Categorization of Escherichia coli outer membrane proteins by dependence on accessory proteins of the β-barrel assembly machinery complex. Thewasano N, Germany EM, Maruno Y, Nakajima Y, Shiota T. J Biol Chem 299 104821 (2023)
  7. Cracking outer membrane biogenesis. Guest RL, Silhavy TJ. Biochim Biophys Acta Mol Cell Res 1870 119405 (2023)
  8. Detergent headgroups control TolC folding in vitro. Ikujuni AP, Budiardjo SJ, Dhar R, Slusky JSG. Biophys J 122 1185-1197 (2023)
  9. Drug Binding to BamA Targets Its Lateral Gate. Kuo KM, Liu J, Pavlova A, Gumbart JC. J Phys Chem B 127 7509-7517 (2023)
  10. Dynamic interplay between the periplasmic chaperone SurA and the BAM complex in outer membrane protein folding. Schiffrin B, Machin JM, Karamanos TK, Zhuravleva A, Brockwell DJ, Radford SE, Calabrese AN. Commun Biol 5 560 (2022)
  11. Modeling intermediates of BamA folding an outer membrane protein. Kuo KM, Ryoo D, Lundquist K, Gumbart JC. Biophys J 121 3242-3252 (2022)
  12. Overexpression of the Bam Complex Improves the Production of Chlamydia trachomatis MOMP in the E. coli Outer Membrane. Huynh DT, Jong WSP, Koningstein GM, van Ulsen P, Luirink J. Int J Mol Sci 23 7393 (2022)
  13. Structural basis of BAM-mediated outer membrane β-barrel protein assembly. Shen C, Chang S, Luo Q, Chan KC, Zhang Z, Luo B, Xie T, Lu G, Zhu X, Wei X, Dong C, Zhou R, Zhang X, Tang X, Dong H. Nature 617 185-193 (2023)
  14. The Escherichia coli outer membrane protein OmpA acquires secondary structure prior to its integration into the membrane. Wang X, Bernstein HD. J Biol Chem 298 101802 (2022)


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