Ultrastable cellulosome-adhesion complex tightens under load

Nature Communications

Volumn 5, Issue , 2014, Pages

  Schoeler, Constantin ^a   Malinowska, Klara H ^a   Bernardi, Rafael C ^b   Milles, Lukas F ^a   Jobst, Markus A ^a   Durner, Ellis ^a   Ott, Wolfgang ^a   Fried, Daniel B ^c   Bayer, Edward A ^c   Schulten, Klaus ^b,d   Gaub, Hermann E ^a   Nash, Michael A ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSOME; CALCIUM; ION; LIGAND; PROTEIN BINDING;

ADHESION; BACTERIUM; BIOMASS; CATALYSIS; CELLULOSE; ENZYME ACTIVITY; PROTEIN; RENEWABLE RESOURCE; SIMULATION; STABILIZATION; STRENGTH;

ARTICLE; ATOMIC FORCE MICROSCOPY; BIOCATALYST; BIOMASS; COVALENT BOND; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RUMINOCOCCUS FLAVEFACIENS; SINGLE MOLECULE FORCE SPECTROSCOPY; BIOPHYSICS; CATALYSIS; CELL ADHESION; CHEMISTRY; COMPUTER SIMULATION; NORMAL DISTRIBUTION; PROTEIN CONFORMATION; PROTEIN FOLDING; RUMINOCOCCUS; SITE DIRECTED MUTAGENESIS;

RUMINOCOCCUS FLAVEFACIENS;

BIOMASS; BIOPHYSICS; CALCIUM; CATALYSIS; CELL ADHESION; CELLULOSOMES; COMPUTER SIMULATION; HYDROGEN BONDING; IONS; LIGANDS; MICROSCOPY, ATOMIC FORCE; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; NORMAL DISTRIBUTION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; RUMINOCOCCUS;

EID: 84923280208     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6635     Document Type: Article

References (51)

1. Doi, R. H. & Kosugi, A. Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat. Rev. Microbiol. 2, 541-551 (2004).
2. Carvalho, A. et al. Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex. Proc. Natl Acad. Sci. USA 100, 13809-13814 (2003).
3. Smith, S. P. & Bayer, E. A. Insights into cellulosome assembly and dynamics: from dissection to reconstruction of the supramolecular enzyme complex. Curr. Opin. Struct. Biol. 23, 686-694 (2013).
4. Bayer, E. A., Lamed, R., White, B. A. & Flint, H. J. From cellulosomes to cellulosomics. Chem. Rec. 8, 364-377 (2008).
5. Demain, A. L., Newcomb, M. & Wu, J. H. D. Cellulase, clostridia, and ethanol. Microbiol. Mol. Biol. Rev. 69, 124-154 (2005).
6. Jindou, S. et al. Cellulosome gene cluster analysis for gauging the diversity of the ruminal cellulolytic bacterium Ruminococcus flavefaciens. FEMS Microbiol. Lett. 285, 188-194 (2008).
7. Ding, S. Y. et al. Cellulosomal scaffoldin-like proteins from Ruminococcus flavefaciens. J. Bacteriol. 183, 1945-1953 (2001).
8. Rincon, M. T. et al. Abundance and diversity of dockerin-containing proteins in the fiber-degrading rumen bacterium, Ruminococcus flavefaciens FD-1. PLoS ONE 5, e12476 (2010).
9. Himmel, M. E. et al. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315, 804-807 (2007).
10. Fierobe, H.-P. et al. Degradation of cellulose substrates by cellulosome chimeras Substrate targeting versus proximity of enzyme components. J. Biol. Chem. 277, 49621-49630 (2002).
11. Valbuena, A. et al. On the remarkable mechanostability of scaffoldins and the mechanical clamp motif. Proc. Natl Acad. Sci. USA 106, 13791-13796 (2009).
12. Salama-Alber, O. et al. Atypical cohesin-dockerin complex responsible for cell-surface attachment of cellulosomal components: binding fidelity, promiscuity, and structural buttresses. J. Biol. Chem. 288, 16827-16838 (2013).
13. Adams, J. J., Webb, B. A., Spencer, H. L. & Smith, S. P. Structural characterization of type ii dockerin module from the cellulosome of Clostridium thermocellum: calcium-induced effects on conformation and target recognition. Biochemistry 44, 2173-2182 (2005).
14. Adams, J. J., Pal, G., Jia, Z. & Smith, S. P. Mechanism of bacterial cell-surface attachment revealed by the structure of cellulosomal type II cohesin-dockerin complex. Proc. Natl Acad. Sci. USA 103, 305-310 (2006).
15. Sikora, M. & Cieplak, M. Mechanical stability of multidomain proteins and novel mechanical clamps. Proteins Struct. Funct. Bioinf. 79, 1786-1799 (2011).
16. Brunecky, R. et al. Structure and function of the Clostridium thermocellum cellobiohydrolase A X1-module repeat: enhancement through stabilization of the CbhA complex. Acta. Crystallogr. 68, 292-299 (2012).
17. Stahl, S. W. et al. Single-molecule dissection of the high-affinity cohesin-dockerin complex. Proc. Natl Acad. Sci. USA 109, 20431-20436 (2012).
18. Jobst, M. A., Schoeler, C., Malinowska, K. & Nash, M. A. Investigating receptor-ligand systems of the cellulosome with AFM-based single-molecule force spectroscopy. J. Vis. Exp. 82, e50950 (2013).
19. Otten, M. et al. From genes to protein mechanics on a chip. Nat. Methods 11, 1127-1130 (2014).
20. Livadaru, L., Netz, R. R. & Kreuzer, H. J. Stretching response of discrete semiflexible polymers. Macromolecules 36, 3732-3744 (2003).
21. Hugel, T., Rief, M., Seitz, M., Gaub, H. & Netz, R. Highly stretched single polymers: atomic-force-microscope experiments versus ab-initio theory. Phys. Rev. Lett. 94, 048301 (2005).
22. Puchner, E. M., Franzen, G., Gautel, M. & Gaub, H. E. Comparing proteins by their unfolding pattern. Biophys. J. 95, 426-434 (2008).
23. Merkel, R., Nassoy, P., Leung, A., Ritchie, K. & Evans, E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature 397, 50-53 (1999).
24. Morfill, J. et al. Affinity-matured recombinant antibody fragments analyzed by single-molecule force spectroscopy. Biophys. J. 93, 3583-3590 (2007).
25. Berkemeier, F. et al. Fast-folding a-helices as reversible strain absorbers in the muscle protein myomesin. Proc. Natl Acad. Sci. USA 108, 14139-14144 (2011).
26. Bertz, M., Wilmanns, M. & Rief, M. The titin-telethonin complex is a directed, superstable molecular bond in the muscle Z-disk. Proc. Natl Acad. Sci. USA 106, 13307-13310 (2009).
27. Marszalek, P. E. et al. Mechanical unfolding intermediates in titin modules. Nature 402, 100-103 (1999).
28. Grandbois, M., Beyer, M., Rief, M., Clausen-Schaumann, H. & Gaub, H. E. How strong is a covalent bond? Science 283, 1727-1730 (1999).
29. Xue, Y., Li, X., Li, H. & Zhang, W. Quantifying thiol-gold interactions towards the efficient strength control. Nat. Commun. 5, 4348 (2014).
30. Bomble, Y. J. et al. Modeling the self-assembly of the cellulosome enzyme complex. J. Biol. Chem. 286, 5614-5623 (2011).
31. Sotomayor, M. & Schulten, K. Single-molecule experiments in vitro and in silico. Science 316, 1144-1148 (2007).
32. Grubmüller, H., Heymann, B. & Tavan, P. Ligand binding: molecular mechanics calculation of the streptavidin biotin rupture force. Science 271, 997-999 (1996).
33. Thomas, W. et al. Catch-bond model derived from allostery explains force-activated bacterial adhesion. Biophys. J. 90, 753-764 (2006).
34. Wang, W. & Malcolm, B. A. Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange site-directed mutagenesis. Biotechniques 26, 680-682 (1999).
35. Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343-345 (2009).
36. Sawano, A. & Miyawaki, A. Directed evolution of green fluorescent protein by a new versatile PCR strategy for site-directed and semi-random mutagenesis. Nucleic Acids Res. 28, e78 (2000).
37. Studier, F. W. Protein production by auto-induction in high-density shaking cultures. Protein Expres. Purif. 41, 207-234 (2005).
38. Zimmermann, J. L., Nicolaus, T., Neuert, G. & Blank, K. Thiol-based, site-specific and covalent immobilization of biomolecules for single-molecule experiments. Nat. Protoc. 5, 975-985 (2010).
39. Yin, J., Lin, A. J., Golan, D. E. & Walsh, C. T. Site-specific protein labeling by Sfp phosphopantetheinyl transferase. Nat. Protoc. 1, 280-285 (2006).
40. Gumpp, H., Stahl, S. W., Strackharn, M., Puchner, E. M. & Gaub, H. E. Ultrastable combined atomic force and total internal fluorescence microscope. Rev. Sci. Instrum. 80, 063704 (2009).
41. Hutter, J. L. & Bechhoefer, J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868 (1993).
42. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graphics 14, 33-38 (1996).
43. Kalé, L. et al. NAMD2: greater scalability for parallel molecular dynamics. J. Comput. Phys. 151, 283-312 (1999).
44. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005).
45. Best, R. B. et al. Optimization of the additive CHARMM All-atom protein force field targeting improved sampling of the backbone f, c and side-chain w 1and w 2dihedral Angles. J. Chem. Theory Comput. 8, 3257-3273 (2012).
46. MacKerell, A. D. et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616 (1998).
47. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-934 (1983).
48. Darden, T., York, D. & Pedersen, L. Particle mesh Ewald: An Nlog(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092 (1993).
49. Izrailev, S., Stepaniants, S., Balsera, M., Oono, Y. & Schulten, K. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72, 1568-1581 (1997).
50. Frishman, D. & Argos, P. Knowledge-based protein secondary structure assignment. Proteins Struct. Funct. Bioinf. 23, 566-579 (1995).
51. Ribeiro, J. V., Tamames, J. A. C., Cerqueira, N. M. F. S. A., Fernandes, P. A. & Ramos, M. J. Volarea-a bioinformatics tool to calculate the surface area and the volume of molecular systems. Chem. Biol. Drug Des. 82, 743-755 (2013).