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Volume 168, Issue 3

What have molecular simulations contributed to understanding of Gram-negative bacterial cell envelopes? Open Access

This article is part of the Bacterial Cell Envelopes collection.

Abstract

Bacterial cell envelopes are compositionally complex and crowded and while highly dynamic in some areas, their molecular motion is very limited, to the point of being almost static in others. Therefore, it is no real surprise that studying them at high resolution across a range of temporal and spatial scales requires a number of different techniques. Details at atomistic to molecular scales for up to tens of microseconds are now within range for molecular dynamics simulations. Here we review how such simulations have contributed to our current understanding of the cell envelopes of Gram-negative bacteria.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacterial cell envelope , membrane protein , molecular dynamics , molecular simulation and periplasm
Funding
This study was supported by the:
  • Bioinformatics Institute, A*STAR (Award Core funds)
    • Principle Award Recipient: PeterJ Bond
  • IBM and EPSRC
    • Principle Award Recipient: CyrilSchroeder
  • Department of Biochemistry, University of Oxford, GB
    • Principle Award Recipient: AnnaL Duncan
  • Engineering and Physical Sciences Research Council (Award EP/R029407/2)
    • Principle Award Recipient: SymaKhalid
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-03-16
2024-04-20
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References

  1. Im W, Khalid S. Molecular simulations of gram-negative bacterial membranes come of age. Annu Rev Phys Chem 2020; 71:171–188 [View Article] [PubMed]
     [Google Scholar]
  2. Khalid S, Piggot TJ, Samsudin F. Atomistic and coarse grain simulations of the cell envelope of gram-negative bacteria: what have we learned?. Acc Chem Res 2019; 52:180–188 [View Article] [PubMed]
     [Google Scholar]
  3. Glass WG, Essex JW, Fraternali F, Gebbie-Rayet J, Marzuoli I et al. Coarse-grained molecular dynamics simulations of membrane proteins: a practical guide. Methods Mol Biol 2021; 2302:253–273 [View Article] [PubMed]
     [Google Scholar]
  4. Souza PCT, Alessandri R, Barnoud J, Thallmair S, Faustino I et al. Martini 3: a general purpose force field for coarse-grained molecular dynamics. Nat Methods 2021; 18:382–388 [View Article] [PubMed]
     [Google Scholar]
  5. Darré L, Machado MR, Brandner AF, González HC, Ferreira S et al. SIRAH: a structurally unbiased coarse-grained force field for proteins with aqueous solvation and long-range electrostatics. J Chem Theory Comput 2015; 11:723–739 [View Article] [PubMed]
     [Google Scholar]
  6. Carpenter TS, Parkin J, Khalid S. The free energy of small solute permeation through the Escherichia coli outer membrane has a distinctly asymmetric profile. J Phys Chem Lett 2016; 7:3446–3451 [View Article] [PubMed]
     [Google Scholar]
  7. Holdbrook DA, Huber RG, Piggot TJ, Bond PJ, Khalid S. Dynamics of crowded vesicles: local and global responses to membrane composition. PLoS One 2016; 11:e0156963 [View Article] [PubMed]
     [Google Scholar]
  8. Chavent M, Duncan AL, Rassam P, Birkholz O, Hélie J et al. How nanoscale protein interactions determine the mesoscale dynamic organisation of bacterial outer membrane proteins. Nat Commun 2018; 9:2846 [View Article] [PubMed]
     [Google Scholar]
  9. Rassam P, Copeland NA, Birkholz O, Tóth C, Chavent M et al. Supramolecular assemblies underpin turnover of outer membrane proteins in bacteria. Nature 2015; 523:333–336 [View Article] [PubMed]
     [Google Scholar]
  10. Benn G, Mikheyeva IV, Inns PG, Forster JC, Ojkic N et al. Phase separation in the outer membrane of Escherichia coli . Proc Natl Acad Sci U S A 2021; 118:118 [View Article] [PubMed]
     [Google Scholar]
  11. Pandit KR, Klauda JB. Membrane models of E. coli containing cyclic moieties in the aliphatic lipid chain. Biochim Biophys Acta 2012; 1818:1205–1210 [View Article] [PubMed]
     [Google Scholar]
  12. Sener MK, Olsen JD, Hunter CN, Schulten K. Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle. Proc Natl Acad Sci U S A 2007; 104:15723–15728 [View Article] [PubMed]
     [Google Scholar]
  13. Hsu PC, Samsudin F, Shearer J, Khalid S. It is complicated: curvature, diffusion, and lipid sorting within the two membranes of Escherichia coli . J Phys Chem Lett 2017; 8:5513–5518 [View Article] [PubMed]
     [Google Scholar]
  14. Vaiwala R, Sharma P, Puranik M, Ayappa KG. Developing a coarse-grained model for bacterial cell walls: evaluating mechanical properties and free energy barriers. J Chem Theory Comput 2020; 16:5369–5384 [View Article] [PubMed]
     [Google Scholar]
  15. Nguyen LT, Gumbart JC, Beeby M, Jensen GJ. Coarse-grained simulations of bacterial cell wall growth reveal that local coordination alone can be sufficient to maintain rod shape. Proc Natl Acad Sci U S A 2015; 112:E3689–98 [View Article] [PubMed]
     [Google Scholar]
  16. Gumbart JC, Ferreira JL, Hwang H, Hazel AJ, Cooper CJ et al. Lpp positions peptidoglycan at the AcrA-TolC interface in the AcrAB-TolC multidrug efflux pump. Biophys J 2021; 120:3973–3982 [View Article] [PubMed]
     [Google Scholar]
  17. Beeby M, Gumbart JC, Roux B, Jensen GJ. Architecture and assembly of the Gram-positive cell wall. Mol Microbiol 2013; 88:664–672 [View Article] [PubMed]
     [Google Scholar]
  18. Burt A, Cassidy CK, Ames P, Bacia-Verloop M, Baulard M et al. Complete structure of the chemosensory array core signalling unit in an E. coli minicell strain. Nat Commun 2020; 11:743 [View Article] [PubMed]
     [Google Scholar]
  19. Hwang H, Paracini N, Parks JM, Lakey JH, Gumbart JC. Distribution of mechanical stress in the Escherichia coli cell envelope. Biochim Biophys Acta Biomembr 2018; 1860:2566–2575 [View Article] [PubMed]
     [Google Scholar]
  20. Jefferies D, Shearer J, Khalid S. Role of O-antigen in response to mechanical stress of the E. coli outer membrane: insights from coarse-grained MD simulations. J Phys Chem B 2019; 123:3567–3575 [View Article] [PubMed]
     [Google Scholar]
  21. O’Donoghue EJ, Sirisaengtaksin N, Browning DF, Bielska E, Hadis M et al. Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog 2017; 13:e1006760 [View Article] [PubMed]
     [Google Scholar]
  22. Jefferies D, Khalid S. To infect or not to infect: molecular determinants of bacterial outer membrane vesicle internalization by host membranes. J Mol Biol 2020; 432:1251–1264 [View Article] [PubMed]
     [Google Scholar]
  23. Koldsø H, Shorthouse D, Hélie J, Sansom MSP. Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers. PLoS Comput Biol 2014; 10:e1003911 [View Article] [PubMed]
     [Google Scholar]
  24. Ewers H, Römer W, Smith AE, Bacia K, Dmitrieff S et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 2010; 12:11–18 [View Article] [PubMed]
     [Google Scholar]
  25. Arora A, Rinehart D, Szabo G, Tamm LK. Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductance states in planar lipid bilayers. J Biol Chem 2000; 275:1594–1600 [View Article] [PubMed]
     [Google Scholar]
  26. Domene C, Bond PJ, Sansom MS. Membrane protein simulations: ion channels and bacterial outer membrane proteins. Adv Protein Chem 2003; 66:159–193 [View Article]
     [Google Scholar]
  27. Bond PJ, Faraldo-Gómez JD, Sansom MSP. OmpA: a pore or not a pore? Simulation and modeling studies. Biophys J 2002; 83:763–775 [View Article]
     [Google Scholar]
  28. Hong H, Szabo G, Tamm LK. Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening. Nat Chem Biol 2006; 2:627–635 [View Article]
     [Google Scholar]
  29. Pongprayoon P, Beckstein O, Wee CL, Sansom MSP. Simulations of anion transport through OprP reveal the molecular basis for high affinity and selectivity for phosphate. Proc Natl Acad Sci U S A 2009; 106:21614–21618 [View Article]
     [Google Scholar]
  30. Chen M, Khalid S, Sansom MSP, Bayley H. Outer membrane protein G: Engineering a quiet pore for biosensing. Proc Natl Acad Sci U S A 2008; 105:6272–6277 [View Article]
     [Google Scholar]
  31. Bond PJ, Derrick JP, Sansom MSP. Membrane simulations of OpcA: gating in the loops?. Biophysical Journal 2007; 92:L23–L25 [View Article] [PubMed]
     [Google Scholar]
  32. Faraldo-Gómez JD, Smith GR, Sansom MSP. Molecular dynamics simulations of the bacterial outer membrane protein FhuA: A comparative study of the ferrichrome-free and bound states. Biophysical Journal 2003; 85:1406–1420 [View Article] [PubMed]
     [Google Scholar]
  33. Cox K, Bond PJ, Grottesi A, Baaden M, Sansom MSP. Outer membrane proteins: comparing X-ray and NMR structures by MD simulations in lipid bilayers. Eur Biophys J 2007; 37:131–141 [View Article] [PubMed]
     [Google Scholar]
  34. Bond PJ, Sansom MSP. Membrane protein dynamics versus environment: simulations of OmpA in a micelle and in a bilayer. Journal of Molecular Biology 2003; 329:1035–1053 [View Article] [PubMed]
     [Google Scholar]
  35. Dhakshnamoorthy B, Ziervogel BK, Blachowicz L, Roux B. A structural study of ion permeation in OmpF porin from anomalous X-ray diffraction and molecular dynamics simulations. J Am Chem Soc 2013; 135:16561–16568 [View Article] [PubMed]
     [Google Scholar]
  36. Im W, Roux B. Ion permeation and selectivity of OmpF porin: a theoretical study based on molecular dynamics, brownian dynamics, and continuum electrodiffusion theory. Journal of Molecular Biology 2002; 322:851–869 [View Article] [PubMed]
     [Google Scholar]
  37. Biró I, Pezeshki S, Weingart H, Winterhalter M, Kleinekathöfer U. Comparing the temperature-dependent conductance of the two structurally similar E. coli Porins OmpC and OmpF. Biophysical Journal 2010; 98:1830–1839 [View Article] [PubMed]
     [Google Scholar]
  38. Kumar A, Hajjar E, Ruggerone P, Ceccarelli M. Structural and dynamical properties of the porins OmpF and OmpC: insights from molecular simulations. J Phys: Condens Matter 2010; 22:454125 [View Article] [PubMed]
     [Google Scholar]
  39. Golla VK, Prajapati JD, Kleinekathöfer U. Millisecond-long simulations of antibiotics transport through outer membrane channels. J Chem Theory Comput 2020; 17:549–559 [View Article] [PubMed]
     [Google Scholar]
  40. Raj Singh P, Ceccarelli M, Lovelle M, Winterhalter M, Mahendran KR. Antibiotic permeation across the ompf channel: modulation of the affinity site in the presence of magnesium. J Phys Chem B 2012; 116:4433–4438 [View Article] [PubMed]
     [Google Scholar]
  41. Pangeni S, Prajapati JD, Bafna J, Nilam M, Nau WM et al. Large-peptide permeation through a membrane channel: understanding protamine translocation through CymA from klebsiella oxytoca*. Angew Chem Int Ed Engl 2021; 60:8089–8094 [View Article] [PubMed]
     [Google Scholar]
  42. Prajapati JD, Kleinekathöfer U, Winterhalter M. How to enter a bacterium: bacterial porins and the permeation of antibiotics. Chem Rev 2021; 121:5158–5192 [View Article] [PubMed]
     [Google Scholar]
  43. Lins RD, Straatsma TP. Computer simulation of the rough lipopolysaccharide membrane of Pseudomonas aeruginosa . Biophys J 2001; 81:1037–1046 [View Article] [PubMed]
     [Google Scholar]
  44. Straatsma TP, Soares TA. Characterization of the outer membrane protein OprF of Pseudomonas aeruginosa in a lipopolysaccharide membrane by computer simulation. Proteins 2009; 74:475–488 [View Article] [PubMed]
     [Google Scholar]
  45. Wu EL, Engstrom O, Jo S, Stuhlsatz D, Wildmalm G et al. Molecular dynamics simulations of E. coli lipopolysaccharide bilayers. Biophysical Journal 2013; 104:586a [View Article]
     [Google Scholar]
  46. Piggot TJ, Holdbrook DA, Khalid S. Electroporation of the E. coli and S. aureus membranes: molecular dynamics simulations of complex bacterial membranes. J Phys Chem B 2011; 115:13381–13388 [View Article]
     [Google Scholar]
  47. Soares TA, Straatsma TP. Assessment of the convergence of molecular dynamics simulations of lipopolysaccharide membranes. Mol Simul 2008; 34:295–307 [View Article]
     [Google Scholar]
  48. Shearer J, Marzinek JK, Bond PJ, Khalid S. Molecular dynamics simulations of bacterial outer membrane lipid extraction: Adequate sampling?. J Chem Phys 2020; 153:044122 [View Article]
     [Google Scholar]
  49. Hsu P-C, Bruininks BMH, Jefferies D, Cesar Telles de Souza P, Lee J et al. CHARMM-GUI Martini Maker for modeling and simulation of complex bacterial membranes with lipopolysaccharides. J Comput Chem 2017; 38:2354–2363 [View Article]
     [Google Scholar]
  50. Lee J, Patel DS, Kucharska I, Tamm LK, Im W. Refinement of OprH-LPS Interactions by Molecular Simulations. Biophys J 2017; 112:346–355 [View Article]
     [Google Scholar]
  51. Piggot TJ, Holdbrook DA, Khalid S. Conformational dynamics and membrane interactions of the E. coli outer membrane protein FecA: a molecular dynamics simulation study. Biochim Biophys Acta 2013; 1828:284–293 [View Article] [PubMed]
     [Google Scholar]
  52. Balusek C, Gumbart JC. Role of the native outer-membrane environment on the transporter BtuB. Biophys J 2016; 111:1409–1417 [View Article] [PubMed]
     [Google Scholar]
  53. Pieńko T, Trylska J. Extracellular loops of BtuB facilitate transport of vitamin B12 through the outer membrane of E. coli. PLoS Comput Biol 2020; 16:e1008024 [View Article] [PubMed]
     [Google Scholar]
  54. Samsudin F, Khalid S. Movement of Arginine through OprD: the energetics of permeation and the role of lipopolysaccharide in directing arginine to the protein. J Phys Chem B 2019; 123:2824–2832 [View Article] [PubMed]
     [Google Scholar]
  55. Kesireddy A, Pothula KR, Lee J, Patel DS, Pathania M et al. Modeling of specific lipopolysaccharide binding sites on a gram-negative porin. J Phys Chem B 2019; 123:5700–5708 [View Article] [PubMed]
     [Google Scholar]
  56. Dong H, Xiang Q, Gu Y, Wang Z, Paterson NG et al. Structural basis for outer membrane lipopolysaccharide insertion. Nature 2014; 511:52–56 [View Article] [PubMed]
     [Google Scholar]
  57. Fiorentino F, Sauer JB, Qiu X, Corey RA, Cassidy CK et al. Dynamics of an LPS translocon induced by substrate and an antimicrobial peptide. Nat Chem Biol 2020; 17:187–195 [View Article] [PubMed]
     [Google Scholar]
  58. Botos I, Majdalani N, Mayclin SJ, McCarthy JG, Lundquist K et al. Structural and functional characterization of the LPS transporter LptDE from gram-negative pathogens. Structure 2016; 24:965–976 [View Article] [PubMed]
     [Google Scholar]
  59. Lundquist KP, Gumbart JC. Presence of substrate aids lateral gate separation in LptD. Biochimica et Biophysica Acta (BBA) - Biomembranes 2020; 1862:183025 [View Article] [PubMed]
     [Google Scholar]
  60. Shrivastava IH, Sansom MSP. Simulations of ion permeation through a potassium channel: molecular dynamics of KcsA in a phospholipid bilayer. Biophysical Journal 2000; 78:557–570 [View Article] [PubMed]
     [Google Scholar]
  61. Allen TW, Kuyucak S, Chung SH. Molecular dynamics study of the KcsA potassium channel. Biophys J 1999; 77:2502–2516 [View Article] [PubMed]
     [Google Scholar]
  62. Grottesi A, Domene C, Hall B, Sansom MSP. Conformational dynamics of M2 helices in KirBac channels: helix flexibility in relation to gating via molecular dynamics simulations. Biochemistry 2005; 44:14586–14594 [View Article] [PubMed]
     [Google Scholar]
  63. Domene C, Grottesi A, Sansom MSP. Filter flexibility and distortion in a bacterial inward rectifier K+ channel: simulation studies of KirBac1.1. Biophys J 2004; 87:256–267 [View Article] [PubMed]
     [Google Scholar]
  64. Jing Z, Rackers JA, Pratt LR, Liu C, Rempe SB et al. Thermodynamics of ion binding and occupancy in potassium channels. Chem Sci 2021; 12:8920–8930 [View Article] [PubMed]
     [Google Scholar]
  65. Mita K, Sumikama T, Iwamoto M, Matsuki Y, Shigemi K et al. Conductance selectivity of Na+ across the K+ channel via Na+ trapped in a tortuous trajectory. Proc Natl Acad Sci U S A 2021; 118:118 [View Article] [PubMed]
     [Google Scholar]
  66. DeMarco KR, Bekker S, Vorobyov I. Challenges and advances in atomistic simulations of potassium and sodium ion channel gating and permeation. J Physiol 2019; 597:679–698 [View Article] [PubMed]
     [Google Scholar]
  67. Mironenko A, Zachariae U, de Groot BL, Kopec W. The persistent question of potassium channel permeation mechanisms. J Mol Biol 2021; 433:167002 [View Article] [PubMed]
     [Google Scholar]
  68. Palmer T, Stansfeld PJ. Targeting of proteins to the twin-arginine translocation pathway. Mol Microbiol 2020; 113:861–871 [View Article] [PubMed]
     [Google Scholar]
  69. Walther TH, Gottselig C, Grage SL, Wolf M, Vargiu AV et al. Folding and self-assembly of the TatA translocation pore based on a charge zipper mechanism. Cell 2013; 152:316–326 [View Article] [PubMed]
     [Google Scholar]
  70. Rodriguez F, Rouse SL, Tait CE, Harmer J, De Riso A et al. Structural model for the protein-translocating element of the twin-arginine transport system. Proc Natl Acad Sci U S A 2013; 110:E1092–101 [View Article] [PubMed]
     [Google Scholar]
  71. Rollauer SE, Tarry MJ, Graham JE, Jääskeläinen M, Jäger F et al. Structure of the TatC core of the twin-arginine protein transport system. Nature 2012; 492:210–214 [View Article] [PubMed]
     [Google Scholar]
  72. Ramasamy S, Abrol R, Suloway CJM, Clemons WM Jr. The glove-like structure of the conserved membrane protein TatC provides insight into signal sequence recognition in twin-arginine translocation. Structure 2013; 21:777–788 [View Article] [PubMed]
     [Google Scholar]
  73. Alcock F, Stansfeld PJ, Basit H, Habersetzer J, Baker MA et al. Assembling the Tat protein translocase. Elife 2016; 5:e20718 [View Article] [PubMed]
     [Google Scholar]
  74. Kusakizako T, Miyauchi H, Ishitani R, Nureki O. Structural biology of the multidrug and toxic compound extrusion superfamily transporters. Biochim Biophys Acta Biomembr 2020; 1862:183154 [View Article] [PubMed]
     [Google Scholar]
  75. Krah A, Huber RG, Zachariae U, Bond PJ. On the ion coupling mechanism of the MATE transporter ClbM. Biochim Biophys Acta Biomembr 2020; 1862:183137 [View Article] [PubMed]
     [Google Scholar]
  76. Leung YM, Holdbrook DA, Piggot TJ, Khalid S. The NorM MATE Transporter from N. gonorrhoeae: Insights into Drug and Ion Binding from Atomistic Molecular Dynamics Simulations. Biophysical Journal 2014; 107:460–468 [View Article] [PubMed]
     [Google Scholar]
  77. Krah A, Zachariae U. Insights into the ion-coupling mechanism in the MATE transporter NorM-VC. Phys Biol 2017; 14:045009 [View Article] [PubMed]
     [Google Scholar]
  78. Jin X, Shao Y, Bai Q, Xue W, Liu H et al. Insights into conformational regulation of PfMATE transporter from Pyrococcus furiosus induced by alternating protonation state of Asp41 residue: A molecular dynamics simulation study. Biochimica et Biophysica Acta (BBA) - General Subjects 2016; 1860:1173–1180 [View Article] [PubMed]
     [Google Scholar]
  79. Ficici E, Zhou W, Castellano S, Faraldo-Gómez JD. Broadly conserved Na+-binding site in the N-lobe of prokaryotic multidrug MATE transporters. Proc Natl Acad Sci U S A 2018; 115:E6172–E6181 [View Article] [PubMed]
     [Google Scholar]
  80. Zakrzewska S, Mehdipour AR, Malviya VN, Nonaka T, Koepke J et al. Inward-facing conformation of a multidrug resistance MATE family transporter. Proc Natl Acad Sci USA 2019; 116:12275–12284 [View Article] [PubMed]
     [Google Scholar]
  81. van den Berg B, Chembath A, Jefferies D, Basle A, Khalid S et al. Structural basis for Mep2 ammonium transceptor activation by phosphorylation. Nat Commun 2016; 7:11337 [View Article] [PubMed]
     [Google Scholar]
  82. Williamson G, Tamburrino A, Bizior M, Boeckstaens G, Dias Mirandela MG et al. Javelle. elife 20209 [View Article]
     [Google Scholar]
  83. Luzhkov VB, Almlöf M, Nervall M, Åqvist J. Computational study of the binding affinity and selectivity of the bacterial ammonium transporter AmtB. Biochemistry 2006; 45:10807–10814 [View Article] [PubMed]
     [Google Scholar]
  84. Yang H, Xu Y, Zhu W, Chen K, Jiang H. Detailed mechanism for AmtB Conducting NH4+/NH3: molecular dynamics simulations. Biophysical Journal 2007; 92:877–885 [View Article] [PubMed]
     [Google Scholar]
  85. Akgun U, Khademi S. Periplasmic vestibule plays an important role for solute recruitment, selectivity, and gating in the Rh/Amt/MEP superfamily. Proc Natl Acad Sci 2011; 108:3970–3975 [View Article] [PubMed]
     [Google Scholar]
  86. Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT et al. Membrane proteins bind lipids selectively to modulate their structure and function. Nature 2014; 510:172–175 [View Article] [PubMed]
     [Google Scholar]
  87. Mirandela GD, Tamburrino G, Hoskisson PA, Zachariae U, Javelle A. The lipid environment determines the activity of the Escherichia coli ammonium transporter AmtB. FASEB J 2019; 33:1989–1999 [View Article] [PubMed]
     [Google Scholar]
  88. Stockner T, Vogel HJ, Tieleman DP. A salt-bridge motif involved in ligand binding and large-scale domain motions of the maltose-binding protein. Biophys J 2005; 89:3362–3371 [View Article] [PubMed]
     [Google Scholar]
  89. Bucher D, Grant BJ, Markwick PR, McCammon JA. Accessing a hidden conformation of the maltose binding protein using accelerated molecular dynamics. PLoS Comput Biol 2011; 7:e1002034 [View Article] [PubMed]
     [Google Scholar]
  90. Kandt C, Xu Z, Tieleman DP. Opening and closing motions in the periplasmic vitamin B12 binding protein BtuF. Biochemistry 2006; 45:13284–13292 [View Article] [PubMed]
     [Google Scholar]
  91. Li H, Cao Z, Hu G, Zhao L, Wang C et al. Ligand-induced structural changes analysis of ribose-binding protein as studied by molecular dynamics simulations. THC 2021; 29:103–114 [View Article] [PubMed]
     [Google Scholar]
  92. Boags AT, Samsudin F, Khalid S. Binding from both sides: TolR and Full-Length OmpA bind and maintain the local structure of the E. coli Cell Wall. Structure 2019; 27:713–724 [View Article] [PubMed]
     [Google Scholar]
  93. Ortiz-Suarez ML, Samsudin F, Piggot TJ, Bond PJ, Khalid S. Full-length OmpA: structure, function, and membrane interactions predicted by molecular dynamics simulations. Biophysical Journal 2016; 111:1692–1702 [View Article] [PubMed]
     [Google Scholar]
  94. Szczepaniak J, Holmes P, Rajasekar K, Kaminska R, Samsudin F et al. The lipoprotein Pal stabilises the bacterial outer membrane during constriction by a mobilisation-and-capture mechanism. Nat Commun 2020; 11:1305 [View Article] [PubMed]
     [Google Scholar]
  95. Samsudin F, Ortiz-Suarez ML, Piggot TJ, Bond PJ, Khalid S. OmpA: a flexible clamp for bacterial cell wall attachment. Structure 2016; 24:2227–2235 [View Article] [PubMed]
     [Google Scholar]
  96. Wojdyla JA, Cutts E, Kaminska R, Papadakos G, Hopper JTS et al. Structure and function of the Escherichia coli Tol-Pal stator protein TolR. J Biol Chem 2015; 290:26675–26687 [View Article] [PubMed]
     [Google Scholar]
  97. Boags A, Samsudin F, Khalid S. Details of hydrophobic entanglement between small molecules and Braun’s lipoprotein within the cavity of the bacterial chaperone LolA. Sci Rep 2019; 9:3717 [View Article] [PubMed]
     [Google Scholar]
  98. Rao S, Bates GT, Matthews CR, Newport TD, Vickery ON et al. Characterizing membrane association and periplasmic transfer of bacterial lipoproteins through molecular dynamics simulations. Structure 2020; 28:475–487 [View Article] [PubMed]
     [Google Scholar]
  99. Lalgudi P, Elcock AH. Molecular dynamics simulations of periplasmic proteins interacting with the peptidoglycan layer of Escherichia coli . Journal of Emerging Investigators 2016
     [Google Scholar]
  100. Pedebos C, Smith IPS, Boags A, Khalid S. The hitchhiker’s guide to the periplasm: Unexpected molecular interactions of polymyxin B1 in E. coli . Structure 2021; 29:444–456 [View Article] [PubMed]
     [Google Scholar]
  101. Ruggerone P, Vargiu AV, Collu F, Fischer N, Kandt C. Molecular dynamics computer simulations of multidrug RND efflux pumps. Comput Struct Biotechnol J 2013; 5:e201302008 [View Article] [PubMed]
     [Google Scholar]
  102. Vargiu AV, Ramaswamy VK, Malloci G, Malvacio I, Atzori A et al. Computer simulations of the activity of RND efflux pumps. Res Microbiol 2018; 169:384–392 [View Article] [PubMed]
     [Google Scholar]
  103. Schulz R, Kleinekathöfer U. Transitions between closed and open conformations of TolC: the effects of ions in simulations. Biophys J 2009; 96:3116–3125 [View Article] [PubMed]
     [Google Scholar]
  104. Raunest M, Kandt C. Locked on one side only: ground state dynamics of the outer membrane efflux duct TolC. Biochemistry 2012; 51:1719–1729 [View Article] [PubMed]
     [Google Scholar]
  105. Vaccaro L, Scott KA, Sansom MSP. Gating at both ends and breathing in the middle: conformational dynamics of TolC. Biophys J 2008; 95:5681–5691 [View Article] [PubMed]
     [Google Scholar]
  106. Jewel Y, Liu J, Dutta P. Coarse-grained simulations of conformational changes in the multidrug efflux transporter AcrB. Mol Biosyst 2017; 13:2006–2014 [View Article] [PubMed]
     [Google Scholar]
  107. Hazel AJ, Abdali N, Leus IV, Parks JM, Smith JC et al. Conformational dynamics of AcrA govern multidrug efflux pump assembly. ACS Infect Dis 2019; 5:1926–1935 [View Article] [PubMed]
     [Google Scholar]
  108. Atzori A, Malloci G, Cardamone F, Bosin A, Vargiu AV et al. Molecular interactions of carbapenem antibiotics with the multidrug efflux transporter AcrB of Escherichia coli . Int J Mol Sci 2020; 21:21 [View Article] [PubMed]
     [Google Scholar]
  109. Collu F, Vargiu AV, Dreier J, Cascella M, Ruggerone P. Recognition of imipenem and meropenem by the RND-transporter MexB studied by computer simulations. J Am Chem Soc 2012; 134:19146–19158 [View Article] [PubMed]
     [Google Scholar]
  110. Bharatham N, Bhowmik P, Aoki M, Okada U, Sharma S et al. Structure and function relationship of OqxB efflux pump from Klebsiella pneumoniae. Nat Commun 2021; 12:5400 [View Article] [PubMed]
     [Google Scholar]
  111. Yeow J, Tan KW, Holdbrook DA, Chong ZS, Marzinek JK et al. The architecture of the OmpC-MlaA complex sheds light on the maintenance of outer membrane lipid asymmetry in Escherichia coli . J Biol Chem 2018; 293:11325–11340 [View Article] [PubMed]
     [Google Scholar]
  112. Abellón-Ruiz J, Kaptan SS, Baslé A, Claudi B, Bumann D et al. Structural basis for maintenance of bacterial outer membrane lipid asymmetry. Nat Microbiol 2017; 2:1616–1623 [View Article] [PubMed]
     [Google Scholar]
  113. Mann D, Fan J, Somboon K, Farrell DP, Muenks A et al. Structure and lipid dynamics in the maintenance of lipid asymmetry inner membrane complex of A. baumannii. Commun Biol 2021; 4:817 [View Article] [PubMed]
     [Google Scholar]
  114. Marrink SJ, Corradi V, Souza PCT, Ingólfsson HI, Tieleman DP et al. Computational modeling of realistic cell membranes. Chem Rev 2019; 119:6184–6226 [View Article] [PubMed]
     [Google Scholar]
  115. Shearer J, Jefferies D, Khalid S. Outer membrane proteins OmpA, FhuA, OmpF, EstA, BtuB, and OmpX have unique lipopolysaccharide fingerprints. J Chem Theory Comput 2019; 15:2608–2619 [View Article] [PubMed]
     [Google Scholar]
  116. Liko I, Degiacomi MT, Lee S, Newport TD, Gault J et al. Lipid binding attenuates channel closure of the outer membrane protein OmpF. Proc Natl Acad Sci U S A 2018; 115:6691–6696 [View Article] [PubMed]
     [Google Scholar]
  117. Gault J, Liko I, Landreh M, Shutin D, Bolla JR et al. Combining native and “omics” mass spectrometry to identify endogenous ligands bound to membrane proteins. Nat Methods 2020; 17:505–508 [View Article] [PubMed]
     [Google Scholar]
  118. Patrick JW, Boone CD, Liu W, Conover GM, Liu Y et al. Allostery revealed within lipid binding events to membrane proteins. Proc Natl Acad Sci U S A 2018; 115:2976–2981 [View Article] [PubMed]
     [Google Scholar]
  119. Bolla JR, Sauer JB, Wu D, Mehmood S, Allison TM et al. Direct observation of the influence of cardiolipin and antibiotics on lipid II binding to MurJ. Nat Chem 2018; 10:363–371 [View Article] [PubMed]
     [Google Scholar]
  120. Gupta K, Donlan JAC, Hopper JTS, Uzdavinys P, Landreh M et al. The role of interfacial lipids in stabilizing membrane protein oligomers. Nature 2017; 541:421–424 [View Article] [PubMed]
     [Google Scholar]
  121. Corey RA, Pyle E, Allen WJ, Watkins DW, Casiraghi M et al. Specific cardiolipin-SecY interactions are required for proton-motive force stimulation of protein secretion. Proc Natl Acad Sci U S A 2018; 115:7967–7972 [View Article] [PubMed]
     [Google Scholar]
  122. Du D, Neuberger A, Orr MW, Newman CE, Hsu PC et al. Interactions of a bacterial RND transporter with a transmembrane small protein in a lipid environment. Structure 2020; 28:625–634 [View Article] [PubMed]
     [Google Scholar]
  123. York A, Lloyd AJ, Genio CID, Shearer J, Hinxman KJ et al. Structure-based modeling and dynamics of MurM, a Streptococcus pneumoniae penicillin resistance determinant present at the cytoplasmic membrane. Structure 2021; 29:731–742 [View Article]
     [Google Scholar]
  124. Corey RA, Song W, Duncan AL, Ansell TB, Sansom MSP et al. Identification and assessment of cardiolipin interactions with E. coli inner membrane proteins. Sci Adv 2021; 7:7 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001165
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What have molecular simulations contributed to understanding of Gram-negative bacterial cell envelopes?
Microbiology 168, 001165 (2022); https://doi.org/10.1099/mic.0.001165
/content/journal/micro/10.1099/mic.0.001165
/content/journal/micro/10.1099/mic.0.001165
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