Insights into cellulosome assembly and dynamics: From dissection to reconstruction of the supramolecular enzyme complex

Current Opinion in Structural Biology

Volumn 23, Issue 5, 2013, Pages 686-694

  Smith, Steven P ^a   Bayer, Edward A ^b  

^a QUEEN S UNIVERSITY   (Canada)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CELLULOSOME; COHESIN; SCAFFOLD PROTEIN; SCAFFOLDIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; BINDING AFFINITY; CARBOHYDRATE BINDING MODULE; CARBOXY TERMINAL SEQUENCE; CIPA SUBUNIT; CLOSTRIDIUM THERMOCELLUM; DOCKERIN MODULE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; SUPRAMOLECULAR ENZYME COMPLEX; X MODULE;

BACTERIA (MICROORGANISMS);

BACTERIA; BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CELLULOSOMES; CHROMOSOMAL PROTEINS, NON-HISTONE; ENZYME ACTIVATION; MULTIENZYME COMPLEXES; PROTEIN BINDING;

EID: 84885856620     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.09.002     Document Type: Review

References (60)

1. Wilson D.B. Microbial diversity of cellulose hydrolysis. Curr Opin Microbiol 2011, 14:259-263.
2. Bayer E.A., Belaich J.P., Shoham Y., Lamed R. The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 2004, 58:521-554.
3. Ding S.Y., Xu Q., Crowley M., Zeng Y., Nimlos M., Lamed R., Bayer E.A., Himmel M.E. A biophysical perspective on the cellulosome: new opportunities for biomass conversion. Curr Opin Biotechnol 2008, 19:218-227.
4. Doi R.H., Kosugi A. Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat Rev Microbiol 2004, 2:541-551.
5. Fontes C.M., Gilbert H.J. Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 2010, 79:655-681.
6. Gilbert H.J. Cellulosomes: microbial nanomachines that display plasticity in quaternary structure. Mol Microbiol 2007, 63:1568-1576.
7. Demain A.L., Newcomb M., Wu J.H. Cellulase, clostridia, and ethanol. Microbiol Mol Biol Rev 2005, 69:124-154.
8. Bayer E.A., Kenig R., Lamed R. Adherence of Clostridium thermocellum to cellulose. J Bacteriol 1983, 156:818-827.
9. Lamed R., Setter E., Bayer E.A. Characterization of a cellulose-binding, cellulase-containing complex in Clostridium thermocellum. J Bacteriol 1983, 156:828-836.
10. Bayer E.A., Chanzy H., Lamed R., Shoham Y. Cellulose, cellulases and cellulosomes. Curr Opin Struct Biol 1998, 8:548-557.
11. Bayer E.A., Lamed R., White B.A., Flint H.J. From cellulosomes to cellulosomics. Chem Rec 2008, 8:364-377.
12. Bayer E.A., Smith S.P., Noach I., Alber O., Adams J.J., Lamed R., Shimon L.J., Frolow F. Can we crystallize a cellulosome?. Biotechology of Lignocellulose Degradation and Biomass Utilization 2009, 183-205. Ito Print Publishing. K. Saaka, S. Karita, T. Kimura, M. Saaka, H. Matsui, H. Miyake, A. Tanaka (Eds.).
13. Gerwig G.J., Kamerling J.P., Vliegenthart J.F., Morag E., Lamed R., Bayer E.A. The nature of the carbohydrate-peptide linkage region in glycoproteins from the cellulosomes of Clostridium thermocellum and Bacteroides cellulosolvens. J Biol Chem 1993, 268:26956-26960.
14. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-D238.
15. Carvalho A.L., Dias F.M., Prates J.A., Nagy T., Gilbert H.J., Davies G.J., Ferreira L.M., Romao M.J., Fontes C.M. Cellulosome assembly revealed by the crystal structure of the cohesin-dockerin complex. Proc Natl Acad Sci U S A 2003, 100:13809-13814.
16. Schaeffer F., Matuschek M., Guglielmi G., Miras I., Alzari P.M., Beguin P. Duplicated dockerin subdomains of Clostridium thermocellum endoglucanase CelD bind to a cohesin domain of the scaffolding protein CipA with distinct thermodynamic parameters and a negative cooperativity. Biochemistry 2002, 41:2106-2114.
17. 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 U S A 2006, 103:305-310.
18. Lemaire M., Miras I., Gounon P., Beguin P. Identification of a region responsible for binding to the cell wall within the S-layer protein of Clostridium thermocellum. Microbiology 1998, 144:211-217.
19. Raman B., McKeown C.K., Rodriguez M., Brown S.D., Mielenz J.R. Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation. BMC Microbiol 2011, 11:134.
20. Raman B., Pan C., Hurst G.B., Rodriguez M., McKeown C.K., Lankford P.K., Samatova N.F., Mielenz J.R. Impact of pretreated Switchgrass and biomass carbohydrates on Clostridium thermocellum ATCC 27405 cellulosome composition: a quantitative proteomic analysis. PLoS ONE 2009, 4:e5271.
21. Pinheiro B.A., Gilbert H.J., Sakka K., Fernandes V.O., Prates J.A., Alves V.D., Bolam D.N., Ferreira L.M., Fontes C.M. Functional insights into the role of novel type I cohesin and dockerin domains from Clostridium thermocellum. Biochem J 2009, 424:375-384.
22. Hemme C.L., Mouttaki H., Lee Y.J., Zhang G., Goodwin L., Lucas S., Copeland A., Lapidus A., Glavina del Rio T., Tice H., et al. Sequencing of multiple clostridial genomes related to biomass conversion and biofuel production. J Bacteriol 2010, 192:6494-6496.
23. Lamed R., Naimark J., Morgenstern E., Bayer E.A. Specialized cell surface structures in cellulolytic bacteria. J Bacteriol 1987, 169:3792-3800.
24. Dassa B., Borovok I., Lamed R., Henrissat B., Coutinho P., Hemme C.L., Huang Y., Zhou J., Bayer E.A. Genome-wide analysis of acetivibrio cellulolyticus provides a blueprint of an elaborate cellulosome system. BMC Genomics 2012, 13:210.
25. Rincon M.T., Dassa B., Flint H.J., Travis A.J., Jindou S., Borovok I., Lamed R., Bayer E.A., Henrissat B., Coutinho P.M., et al. Abundance and diversity of dockerin-containing proteins in the fiber-degrading rumen bacterium, Ruminococcus flavefaciens FD-1. PLoS ONE 2010, 5:e12476.
26. Lytle B.L., Volkman B.F., Westler W.M., Heckman M.P., Wu J.H. Solution structure of a type I dockerin domain, a novel prokaryotic, extracellular calcium-binding domain. J Mol Biol 2001, 307:745-753.
27. Shimon L.J., Bayer E.A., Morag E., Lamed R., Yaron S., Shoham Y., Frolow F. A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly. Structure 1997, 5:381-390.
28. Tavares G.A., Beguin P., Alzari P.M. The crystal structure of a type I cohesin domain at 1.7Å resolution. J Mol Biol 1997, 273:701-713.
29. Tormo J., Lamed R., Chirino A.J., Morag E., Bayer E.A., Shoham Y., Steitz T.A. Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. EMBO J 1996, 15:5739-5751.
30. Yaniv O., Morag E., Borovok I., Bayer E.A., Lamed R., Frolow F., Shimon L.J. Structure of a family 3a carbohydrate-binding module from the cellulosomal scaffoldin CipA of Clostridium thermocellum with flanking linkers: implications for cellulosome structure. Acta Cryst F Struct Biol Cryst Commun 2013, 69:733-737.
31. Carvalho A.L., Pires V.M., Gloster T.M., Turkenburg J.P., Prates J.A., Ferreira L.M., Romao M.J., Davies G.J., Fontes C.M., Gilbert H.J. Insights into the structural determinants of cohesin-dockerin specificity revealed by the crystal structure of the type II cohesin from Clostridium thermocellum SdbA. J Mol Biol 2005, 349:909-915.
32. Carvalho A.L., Dias F.M., Nagy T., Prates J.A., Proctor M.R., Smith N., Bayer E.A., Davies G.J., Ferreira L.M., Romao M.J., et al. Evidence for a dual binding mode of dockerin modules to cohesins. Proc Natl Acad Sci U S A 2007, 104:3089-3094.
33. Pinheiro B.A., Proctor M.R., Martinez-Fleites C., Prates J.A., Money V.A., Davies G.J., Bayer E.A., Fontesm C.M., Fierobe H.P., Gilbert H.J. The Clostridium cellulolyticum dockerin displays a dual binding mode for its cohesin partner. J Biol Chem 2008, 283:18422-18430.
34. Stahl S.W., Nash M.A., Fried D.B., Slutzki M., Barak Y., Bayer E.A., Gaub H.E. Single-molecule dissection of the high-affinity cohesin-dockerin complex. Proc Natl Acad Sci U S A 2012, 109:20431-20436.
35. Bras J.L., Alves V.D., Carvalho A.L., Najmudin S., Prates J.A., Ferreira L.M., Bolam D.N., Romao M.J., Gilbert H.J., Fontes C.M. Novel Clostridium thermocellum type I cohesin-dockerin complexes reveal a single binding mode. J Biol Chem 2012, 287:44394-44405.
36. Karpol A., Jobby M.K., Slutzki M., Noach I., Chitayat S., Smith S.P., Bayer E.A. Structural and functional characterization of a novel type-III dockerin from Ruminococcus flavefaciens. FEBS Lett 2013, 587:30-36.
37. Salama-Alber O., Jobby M.K., Chitayat S., Smith S.P., White B.A., Shimon L.J., Lamed R., Frolow F., Bayer E.A. Atypical cohesin-dockerin complex responsible for cell-surface attachment of cellulosomal components: binding fidelity, promiscuity, and structural buttresses. J Biol Chem 2013, 288:16827-16838.
38. Alber O., Noach I., Rincon M.T., Flint H.J., Shimon L.J., Lamed R., Frolow F., Bayer E.A. Cohesin diversity revealed by the crystal structure of the anchoring cohesin from Ruminococcus flavefaciens. Proteins 2009, 77:699-709.
39. Peer A., Smith S.P., Bayer E.A., Lamed R., Borovok I. Noncellulosomal cohesin- and dockerin-like modules in the three domains of life. FEMS Microbiol Lett 2009, 291:1-16.
40. Adams J.J., Gregg K., Bayer E.A., Boraston A.B., Smith S.P. Structural basis of Clostridium perfringens toxin complex formation. Proc Natl Acad Sci U S A 2008, 105:12194-12199.
41. Chitayat S., Adams J.J., Furness H.S., Bayer E.A., Smith S.P. The solution structure of the C-terminal modular pair from Clostridium perfringens mu-toxin reveals a noncellulosomal dockerin module. J Mol Biol 2008, 381:1202-1212.
42. Chitayat S., Gregg K., Adams J.J., Ficko-Blean E., Bayer E.A., Boraston A.B., Smith S.P. Three-dimensional structure of a putative non-cellulosomal cohesin module from a Clostridium perfringens family 84 glycoside hydrolase. J Mol Biol 2008, 375:20-28.
43. Bras J.L., Cartmell A., Carvalho A.L., Verze G., Bayer E.A., Vazana Y., Correia M.A., Prates J.A., Ratnaparkhe S., Boraston A.B., et al. Structural insights into a unique cellulase fold and mechanism of cellulose hydrolysis. Proc Natl Acad Sci U S A 2011, 108:5237-5242.
44. Levy-Assaraf M., Voronov-Goldman M., Rozman Grinberg I., Weiserman G., Shimon L.J., Jindou S., Borovok I., White B.A., Bayer E.A., Lamed R., Frolow F. Crystal structure of an uncommon cellulosome-related protein module from Ruminococcus flavefaciens that resembles papain-like cysteine peptidases. PLoS ONE 2013, 8:e56138.
45. Cuiv P.O., Gupta R., Goswami H.P., Morrison M. Extending the cellulosome paradigm: the modular Clostridium thermocellum cellulosomal serpin, PinA, is a broad spectrum inhibitor of subtilisin like proteases. Appl Environ Microbiol 2013, 10.1128/AEM.01912-13.
46. Kang S., Barak Y., Lamed R., Bayer E.A., Morrison M. The functional repertoire of prokaryote cellulosomes includes the serpin superfamily of serine proteinase inhibitors. Mol Microbiol 2006, 60:1344-1354.
47. Zverlov V.V., Kellermann J., Schwarz W.H. Functional subgenomics of Clostridium thermocellum cellulosomal genes: identification of the major catalytic components in the extracellular complex and detection of three new enzymes. Proteomics 2005, 5:3646-3653.
48. Caspi J., Barak Y., Haimovitz R., Gilary H., Irwin D.C., Lamed R., Wilson D.B., Bayer E.A. Thermobifida fusca exoglucanase Cel6B is incompatible with the cellulosomal mode in contrast to endoglucanase Cel6A. Syst Synth Biol 2010, 4:193-201.
49. Mayer F., Coughlan M.P., Mori Y., Ljungdahl L.G. Macromolecular organization of the cellulolytic enzyme complex of Clostridium thermocellum as revealed by electron microscopy. Appl Environ Microbiol 1987, 53:2785-2792.
50. Czjzek M., Fierobe H.P., Receveur-Brechot V. Small-angle X-ray scattering and crystallography: a winning combination for exploring the multimodular organization of cellulolytic macromolecular complexes. Methods Enzymol 2012, 510:183-210.
51. Bomble Y.J., Beckham G.T., Matthews J.F., Nimlos M.R., Himmel M.E., Crowley M.F. Modeling the self-assembly of the cellulosome enzyme complex. J Biol Chem 2011, 286:5614-5623.
52. Currie M.A., Adams J.J., Faucher F., Bayer E.A., Jia Z., Smith S.P. Scaffoldin conformation and dynamics revealed by a ternary complex from the Clostridium thermocellum cellulosome. J Biol Chem 2012, 287:26953-26961.
53. Currie M.A., Cameron K., Dias F.M., Spencer H.L., Bayer E.A., Fontes C.M., Smith S.P., Jia Z. Small angle X-ray scattering analysis of Clostridium thermocellum cellulosome N-terminal complexes reveals a highly dynamic structure. J Biol Chem 2013, 288:7978-7985.
54. Garcia-Alvarez B., Melero R., Dias F.M., Prates J.A., Fontes C.M., Smith S.P., Romao M.J., Carvalho A.L., Llorca O. Molecular architecture and structural transitions of a Clostridium thermocellum mini-cellulosome. J Mol Biol 2011, 407:571-580.
55. Hammel M., Fierobe H.P., Czjzek M., Finet S., Receveur-Brechot V. Structural insights into the mechanism of formation of cellulosomes probed by small angle X-ray scattering. J Biol Chem 2004, 279:55985-57985.
56. Hammel M., Fierobe H.P., Czjzek M., Kurkal V., Smith J.C., Bayer E.A., Finet S., Receveur-Brechot V. Structural basis of cellulosome efficiency explored by small angle X-ray scattering. J Biol Chem 2005, 280:38562-38568.
57. Noach I., Levy-Assaraf M., Lamed R., Shimon L.J., Frolow F., Bayer E.A. Modular arrangement of a cellulosomal scaffoldin subunit revealed from the crystal structure of a cohesin dyad. J Mol Biol 2010, 399:294-305.
58. Molinier A.L., Nouailler M., Valette O., Tardif C., Receveur-Brechot V., Fierobe H.P. Synergy, structure and conformational flexibility of hybrid cellulosomes displaying various inter-cohesins linkers. J Mol Biol 2011, 405:143-157.
59. Adams J.J., Currie M.A., Ali S., Bayer E.A., Jia Z., Smith S.P. Insights into higher-order organization of the cellulosome revealed by a dissect-and-build approach: crystal structure of interacting Clostridium thermocellum multimodular components. J Mol Biol 2010, 396:833-839.
60. Alzari P.M., Souchon H., Dominquez R. The crystal structure of endoglucanase CelA, a family 8 glycosyl hydrolase from Clostridium thermocellum. Structure 1996, 4:265-275.