Entropic Bonding of the Type 1 Pilus from Experiment and Simulation

Overview

Journal R Soc Open Sci

Specialty Science

Date 2020 May 21

PMID 32431906

Citations 1

Authors

Fabiano Corsetti

Alvaro Alonso-Caballero

Simon Poly

Raul Perez-Jimenez

Emilio Artacho

Affiliations

Soon will be listed here.

Abstract

The type 1 pilus is a bacterial filament consisting of a long coiled proteic chain of subunits joined together by non-covalent bonding between complementing -strands. Its strength and structural stability are critical for its anchoring function in uropathogenic bacteria. The pulling and unravelling of the FimG subunit of the pilus was recently studied by atomic force microscopy experiments and steered molecular dynamics simulations (Alonso-Caballero 2018 . , 2758. (doi:10.1038/s41467-018-05107-6)). In this work, we perform a quantitative comparison between experiment and simulation, showing a good agreement in the underlying work values for the unfolding. The simulation results are then used to estimate the free energy difference for the detachment of FimG from the complementing strand of the neighbouring subunit in the chain, FimF. Finally, we show that the large free energy difference for the unravelling and detachment of the subunits which leads to the high stability of the chain is entirely entropic in nature.

Citing Articles

Entropic bonding of the type 1 pilus from experiment and simulation.

Corsetti F, Alonso-Caballero A, Poly S, Perez-Jimenez R, Artacho E R Soc Open Sci. 2020; 7(4):200183.

PMID: 32431906 PMC: 7211842. DOI: 10.1098/rsos.200183.

References

Best R, Li B, Steward A, Daggett V, Clarke J . Can non-mechanical proteins withstand force? Stretching barnase by atomic force microscopy and molecular dynamics simulation. Biophys J. 2001; 81(4):2344-56. PMC: 1301705. DOI: 10.1016/S0006-3495(01)75881-X. View

Gore J, Ritort F, Bustamante C . Bias and error in estimates of equilibrium free-energy differences from nonequilibrium measurements. Proc Natl Acad Sci U S A. 2003; 100(22):12564-9. PMC: 240657. DOI: 10.1073/pnas.1635159100. View

Ritort F . Single-molecule experiments in biological physics: methods and applications. J Phys Condens Matter. 2011; 18(32):R531-83. DOI: 10.1088/0953-8984/18/32/R01. View

Isralewitz B, Gao M, Schulten K . Steered molecular dynamics and mechanical functions of proteins. Curr Opin Struct Biol. 2001; 11(2):224-30. DOI: 10.1016/s0959-440x(00)00194-9. View

Phillips J, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E . Scalable molecular dynamics with NAMD. J Comput Chem. 2005; 26(16):1781-802. PMC: 2486339. DOI: 10.1002/jcc.20289. View

Crooks G . Entropy production fluctuation theorem and the nonequilibrium work relation for free energy differences. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 2002; 60(3):2721-6. DOI: 10.1103/physreve.60.2721. View

Huggins D . Quantifying the entropy of binding for water molecules in protein cavities by computing correlations. Biophys J. 2015; 108(4):928-936. PMC: 4336375. DOI: 10.1016/j.bpj.2014.12.035. View

Borgia A, Williams P, Clarke J . Single-molecule studies of protein folding. Annu Rev Biochem. 2008; 77:101-25. DOI: 10.1146/annurev.biochem.77.060706.093102. View

Hospenthal M, Waksman G . The Remarkable Biomechanical Properties of the Type 1 Chaperone-Usher Pilus: A Structural and Molecular Perspective. Microbiol Spectr. 2019; 7(1). PMC: 11588285. DOI: 10.1128/microbiolspec.PSIB-0010-2018. View

10.

Meissner R, Wei G, Ciacchi L . Estimation of the free energy of adsorption of a polypeptide on amorphous SiO2 from molecular dynamics simulations and force spectroscopy experiments. Soft Matter. 2015; 11(31):6254-65. DOI: 10.1039/c5sm01444a. View

11.

Manosas M, Ritort F . Thermodynamic and kinetic aspects of RNA pulling experiments. Biophys J. 2005; 88(5):3224-42. PMC: 1305472. DOI: 10.1529/biophysj.104.045344. View

12.

Wright K, Seed P, Hultgren S . Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol. 2007; 9(9):2230-41. DOI: 10.1111/j.1462-5822.2007.00952.x. View

13.

Geibel S, Procko E, Hultgren S, Baker D, Waksman G . Structural and energetic basis of folded-protein transport by the FimD usher. Nature. 2013; 496(7444):243-6. PMC: 3673227. DOI: 10.1038/nature12007. View

14.

Carrion-Vazquez M, Oberhauser A, FOWLER S, Marszalek P, Broedel S, Clarke J . Mechanical and chemical unfolding of a single protein: a comparison. Proc Natl Acad Sci U S A. 1999; 96(7):3694-9. PMC: 22356. DOI: 10.1073/pnas.96.7.3694. View

15.

Narayanan C, Dias C . Hydrophobic interactions and hydrogen bonds in β-sheet formation. J Chem Phys. 2013; 139(11):115103. DOI: 10.1063/1.4821596. View

16.

Mikulska K, Strzelecki J, Nowak W . Nanomechanics of β-rich proteins related to neuronal disorders studied by AFM, all-atom and coarse-grained MD methods. J Mol Model. 2014; 20(3):2144. PMC: 3964301. DOI: 10.1007/s00894-014-2144-5. View

17.

Hutchinson E, Thornton J . HERA--a program to draw schematic diagrams of protein secondary structures. Proteins. 1990; 8(3):203-12. DOI: 10.1002/prot.340080303. View

18.

Smith S, Cui Y, Bustamante C . Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science. 1996; 271(5250):795-9. DOI: 10.1126/science.271.5250.795. View

19.

Klimov D, Thirumalai D . Native topology determines force-induced unfolding pathways in globular proteins. Proc Natl Acad Sci U S A. 2000; 97(13):7254-9. PMC: 16532. DOI: 10.1073/pnas.97.13.7254. View

20.

Fisher T, Oberhauser A, Carrion-Vazquez M, Marszalek P, Fernandez J . The study of protein mechanics with the atomic force microscope. Trends Biochem Sci. 1999; 24(10):379-84. DOI: 10.1016/s0968-0004(99)01453-x. View