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Ligand-gated diffusion across the bacterial outer membrane.

Lepore BW, Indic M, Pham H, Hearn EM, Patel DR, van den Berg B
Proc Natl Acad Sci U S A 108 10121-6 (2011)
Related entries: 2r89, 2r8a, 3pf1, 3pgr, 3pgs

Cited: 35 times
EuropePMC logo PMID: 21593406

Abstract

Ligand-gated channels, in which a substrate transport pathway is formed as a result of the binding of a small-molecule chemical messenger, constitute a diverse class of membrane proteins with important functions in prokaryotic and eukaryotic organisms. Despite their widespread nature, no ligand-gated channels have yet been found within the outer membrane (OM) of Gram-negative bacteria. Here we show, using in vivo transport assays, intrinsic tryptophan fluorescence and X-ray crystallography, that high-affinity (submicromolar) substrate binding to the OM long-chain fatty acid transporter FadL from Escherichia coli causes conformational changes in the N terminus that open up a channel for substrate diffusion. The OM long-chain fatty acid transporter FadL from E. coli is a unique paradigm for OM diffusion-driven transport, in which ligand gating within a β-barrel membrane protein is a prerequisite for channel formation.

Articles - 3pgu mentioned but not cited (1)

  1. Ligand-gated diffusion across the bacterial outer membrane. Lepore BW, Indic M, Pham H, Hearn EM, Patel DR, van den Berg B. Proc Natl Acad Sci U S A 108 10121-10126 (2011)


Reviews citing this publication (5)

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  5. Degradation of Exogenous Fatty Acids in Escherichia coli. Pavoncello V, Barras F, Bouveret E. Biomolecules 12 1019 (2022)

Articles citing this publication (29)

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  2. Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. Kamp HD, Patimalla-Dipali B, Lazinski DW, Wallace-Gadsden F, Camilli A. PLoS Pathog 9 e1003800 (2013)
  3. Substrate specificity within a family of outer membrane carboxylate channels. Eren E, Vijayaraghavan J, Liu J, Cheneke BR, Touw DS, Lepore BW, Indic M, Movileanu L, van den Berg B. PLoS Biol 10 e1001242 (2012)
  4. A Peptidomimetic Antibiotic Targets Outer Membrane Proteins and Disrupts Selectively the Outer Membrane in Escherichia coli. Urfer M, Bogdanovic J, Lo Monte F, Moehle K, Zerbe K, Omasits U, Ahrens CH, Pessi G, Eberl L, Robinson JA. J Biol Chem 291 1921-1932 (2016)
  5. The Escherichia coli Phospholipase PldA Regulates Outer Membrane Homeostasis via Lipid Signaling. May KL, Silhavy TJ. mBio 9 e00379-18 (2018)
  6. Rhizobial homologs of the fatty acid transporter FadL facilitate perception of long-chain acyl-homoserine lactone signals. Krol E, Becker A. Proc Natl Acad Sci U S A 111 10702-10707 (2014)
  7. Unsaturated long chain free fatty acids are input signals of the Salmonella enterica PhoP/PhoQ regulatory system. Viarengo G, Sciara MI, Salazar MO, Kieffer PM, Furlán RL, García Véscovi E. J Biol Chem 288 22346-22358 (2013)
  8. Antagonistic Pleiotropy in the Bifunctional Surface Protein FadL (OmpP1) during Adaptation of Haemophilus influenzae to Chronic Lung Infection Associated with Chronic Obstructive Pulmonary Disease. Moleres J, Fernández-Calvet A, Ehrlich RL, Martí S, Pérez-Regidor L, Euba B, Rodríguez-Arce I, Balashov S, Cuevas E, Liñares J, Ardanuy C, Martín-Santamaría S, Ehrlich GD, Mell JC, Garmendia J. mBio 9 e01176-18 (2018)
  9. How hydrophobic molecules traverse the outer membranes of gram-negative bacteria. Wiener MC, Horanyi PS. Proc Natl Acad Sci U S A 108 10929-10930 (2011)
  10. Substrate uptake and subcellular compartmentation of anoxic cholesterol catabolism in Sterolibacterium denitrificans. Lin CW, Wang PH, Ismail W, Tsai YW, El Nayal A, Yang CY, Yang FC, Wang CH, Chiang YR. J Biol Chem 290 1155-1169 (2015)
  11. Improving Escherichia coli membrane integrity and fatty acid production by expression tuning of FadL and OmpF. Tan Z, Black W, Yoon JM, Shanks JV, Jarboe LR. Microb Cell Fact 16 38 (2017)
  12. An outer membrane protein undergoes enthalpy- and entropy-driven transitions. Cheneke BR, Indic M, van den Berg B, Movileanu L. Biochemistry 51 5348-5358 (2012)
  13. Structural and thermodynamic characterization of the interaction between two periplasmic Treponema pallidum lipoproteins that are components of a TPR-protein-associated TRAP transporter (TPAT). Brautigam CA, Deka RK, Schuck P, Tomchick DR, Norgard MV. J Mol Biol 420 70-86 (2012)
  14. A genome-wide screen in Escherichia coli reveals that ubiquinone is a key antioxidant for metabolism of long-chain fatty acids. Agrawal S, Jaswal K, Shiver AL, Balecha H, Patra T, Chaba R. J Biol Chem 292 20086-20099 (2017)
  15. Uptake and trans-membrane transport of petroleum hydrocarbons by microorganisms. Hua F, Wang HQ. Biotechnol Biotechnol Equip 28 165-175 (2014)
  16. Structural basis for chitin acquisition by marine Vibrio species. Aunkham A, Zahn M, Kesireddy A, Pothula KR, Schulte A, Baslé A, Kleinekathöfer U, Suginta W, van den Berg B. Nat Commun 9 220 (2018)
  17. Functional characterization of ExFadLO, an outer membrane protein required for exporting oxygenated long-chain fatty acids in Pseudomonas aeruginosa. Martínez E, Estupiñán M, Pastor FI, Busquets M, Díaz P, Manresa A. Biochimie 95 290-298 (2013)
  18. Positive regulation of the Shewanella oneidensis OmpS38, a major porin facilitating anaerobic respiration, by Crp and Fur. Gao T, Ju L, Yin J, Gao H. Sci Rep 5 14263 (2015)
  19. Synthesis and antimicrobial activity against Pseudomonas aeruginosa of macrocyclic β-hairpin peptidomimetic antibiotics containing N-methylated amino acids. Vetterli SU, Moehle K, Robinson JA. Bioorg Med Chem 24 6332-6339 (2016)
  20. Crystal structure of a COG4313 outer membrane channel. van den Berg B, Bhamidimarri SP, Winterhalter M. Sci Rep 5 11927 (2015)
  21. Structural biology: Lipopolysaccharide rolls out the barrel. Bishop RE. Nature 511 37-38 (2014)
  22. Modulating the import of medium-chain alkanes in E. coli through tuned expression of FadL. Call TP, Akhtar MK, Baganz F, Grant C. J Biol Eng 10 5 (2016)
  23. Enhancing poly(3-hydroxyalkanoate) production in Escherichia coli by the removal of the regulatory gene arcA. Scheel RA, Ji L, Lundgren BR, Nomura CT. AMB Express 6 120 (2016)
  24. Theoretical analysis of ion conductance and gating transitions in the OpdK (OccK1) channel. Pothula KR, Kleinekathöfer U. Analyst 140 4855-4864 (2015)
  25. Uptake of monoaromatic hydrocarbons during biodegradation by FadL channel-mediated lateral diffusion. Somboon K, Doble A, Bulmer D, Baslé A, Khalid S, van den Berg B. Nat Commun 11 6331 (2020)
  26. Inward-facing glycine residues create sharp turns in β-barrel membrane proteins. Zhang Z, Ryoo D, Balusek C, Acharya A, Rydmark MO, Linke D, Gumbart JC. Biochim Biophys Acta Biomembr 1863 183662 (2021)
  27. GFP Scaffold-Based Engineering for the Production of Unbranched Very Long Chain Fatty Acids in Escherichia coli With Oleic Acid and Cerulenin Supplementation. Kassab E, Mehlmer N, Brueck T. Front Bioeng Biotechnol 7 408 (2019)
  28. Optimizing a Fed-Batch High-Density Fermentation Process for Medium Chain-Length Poly(3-Hydroxyalkanoates) in Escherichia coli. Scheel RA, Ho T, Kageyama Y, Masisak J, McKenney S, Lundgren BR, Nomura CT. Front Bioeng Biotechnol 9 618259 (2021)
  29. Efficient Biosynthesis of 10-Hydroxy-2-decenoic Acid Using a NAD(P)H Regeneration P450 System and Whole-Cell Catalytic Biosynthesis. Wang L, Wang L, Wang R, Wang Z, Wang J, Yuan H, Su J, Li Y, Yang S, Han T. ACS Omega 7 17774-17783 (2022)


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