Cellulose, cellulases and cellulosomes

Current Opinion in Structural Biology

Volumn 8, Issue 5, 1998, Pages 548-557

  Bayer, Edward A ^a   Chanzy, Henri ^b   Lamed, Raphael ^c   Shoham, Yuval ^d  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b CENTRE DE RECHERCHES SUR LES MACROMOLÉCULES VÉGÉTALES CERMAV CNRS   (France)

^c TEL AVIV UNIVERSITY   (Israel)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULASE; CELLULOSE;

BACTERIAL METABOLISM; CARBOHYDRATE ANALYSIS; COMPLEX FORMATION; HYDROLYSIS; PRIORITY JOURNAL; REVIEW;

BACTERIA (MICROORGANISMS);

EID: 0031764782     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(98)80143-7     Document Type: Article

References (66)

1. Henrissat B, Davies G. Structural and sequence-based classification of glycoside hydrolases. of special interest Curr Opin Struct Biol. 7:1997;637-644 An excellent review of the various modes of classification of the glycoside hydrolases, which include cellulases and related enzymes. The review describes the accelerating number of sequences and 3D structures that have been determined for these enzymes, as well as new insights into their properties and improved methodologies for identifying their catalytic residues. The authors discuss the limitations of conventional classification schemes and summarize more recent complementary approaches of greater relevance in categorizing the enzymes that hydrolyze oligosaccharides and polysaccharides.
2. of outstanding interest Claeyssens M, Nerinckx W, Piens K. Carbohydrases from Trichoderma reesei and Other Microorganisms. Structures, Biochemistry and Applications. 1998;The Royal Society of Chemistry, Cambridge, A collection of over 30 excellent articles and reviews that describe the contemporary status of fungal and bacterial cellulases, and related enzymes. The chapters were authored by the invited lecturers at the 3rd Tricel Meeting (August 1997; Ghent, Belgium). The contributions were composed after the meeting and many of the chapters reflect the fresh interaction among the participants. The articles are distinguished by their concern with structural and mechanistic detail on the molecular level, which characterizes the progress in this area. The book is highly recommended for both newcomers to the field, as well as established researchers.
3. Viikari L, Teeri T. Biochemistry and genetics of cellulases and hemicellulases and their application. J Biotechnol. 57:1997;1-228.
4. O'Sullivan AC. Cellulose: the structure slowly unravels. of special interest Cellulose. 4:1997;173-207 This well-written review provides a good literature survey, describing the slow unraveling of the fine structure of cellulose. The review is of particular interest as it is the only one that summarizes recent reports in this field up to 1995.
5. Krässig HA. Cellulose, Structure, Accessibility and Reactivity. 1993;Gordon and Breach Science, Yverdon.
6. Brown MR Jr. The biosynthesis of cellulose. J Macromol Sci - Pure Appl Chem. A33:1996;1345-1373.
7. Hieta K, Kuga S, Usuda M. Electron staining of reducing ends evidences a parallel-chain structure in Valonia cellulose. Biopolymers. 23:1984;1807-1810.
8. Chanzy H, Henrissat B. Unidirectional degradation of Valonia cellulose microcrystals subjected to cellulase action. FEBS Lett. 184:1985;285-288.
9. Sarko A, Muggli R. Packing analysis of carbohydrates and polysaccharides. III. Valonia cellulose and cellulose II. Macromolecules. 7:1974;486-494.
10. Gardner KH, Blackwell J. The structure of native cellulose. Biopolymers. 13:1974;1975-2001.
11. French AD, Howley PS. Comparisons of structures proposed for cellulose. Schuerch C. Cellulose and Wood. Chemistry and Technology. 1989;159-167 Interscience, New York.
12. Atalla RH, VanderHart DL. Native cellulose: a composite of two distinct crystalline forms. Science. 223:1984;283-285.
13. β are packed in the 'parallel-up' manner. The use of the same technique also proves that cellulose biosynthesis occurs at the nonreducing end of the growing cellulose chains.
14. Sugiyama J, Harada H, Fujiyoshi Y, Uyeda N. High resolution observations of cellulose microfibrils. Mokuzai Gakkaishi. 30:1984;98-99.
15. Revol JF, Goring DAI. Directionality of the fibre c-axis of cellulose crystallites in microfibrils of Valonia ventricosa. Polymer. 24:1983;1547-1550.
16. Chanzy H. Aspects of cellulose structure. Kennedy JF, Phillips GO, Williams PA. Cellulose Sources and Exploitation, Industrial Utilization, Biotechnology and Physiscochemical Properties. 1990;3-12 Ellis Horwood, New York.
17. 13C NMR investigation of molecular ordering in celluloses. Carbohydr Res. 302:1997;19-25.
18. Sugiyama J, Vuong R, Chanzy H. Electron diffraction study of the two crystalline phases occurring in native cellulose from an algal cell wall. Macromolecules. 24:1991;4168-4175.
19. β phase.
20. Sassi J-F. Etude structurale de l'acétylation de la cellulose. Application à la préparation de nanocomposites. PhD Thesis. 1995;Joseph Fourier University of Grenoble, Grenoble, France.
21. Baker A, Helbert W, Sugiyama J, Miles M. High-resolution atomic force microscopy of native Valonia cellulose I microcrystals. of special interest J Struct Biol. 119:1997;129-138 The surface of Valonia cellulose was visualized under water or propanol, with a clear resolution of 0.5 nm, revealing the glucosyl moieties of cellulose surface chains.
22. Henrissat B, Teeri TT, Warren RAJ. A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett. 425:1998;352-354.
23. Sulzenbacher G, Shareck F, Morosoli R, Dupont C, Davies G. The Streptomyces lividans family 12 endoglucanase: construction of the catalytic core, expression, and X-ray structure at 1.75 Å resolution. of outstanding interest Biochemistry. 36:1997;16032-16039 This article provides the first structural description of a family 12 member, which had previously eluded detailed structural analysis. The folding motif and catalytic machinery of this enzyme clearly demonstrate the previously predicted similarity to the family 11 xylanases. The molecular basis for substrate specificity - cellulose versus xylan for the family 12 and family 11 enzymes, respectively - is suggested on the basis of comparative active site architectures.
24. Reverbel-Leroy C, Pagés S, Belaich A, Belaich J-P, Tardif C. The processive endocellulase CelF, a major component of the Clostridium cellulolyticum cellulosome: Purification and characterization of the recombinant form. J Bacteriol. 179:1997;46-52.
25. Parsiegla G, Juy M, Reverbel-Leroy C, Tardif C, Belaich J-P, Driguez H, Haser R. The crystal structure of the processive endonuclease CelF of Clostridium cellulolyticum in complex with a thiooligosaccharide inhibitor at 2.0 Å resolution. EMBO J. 1998;. in press.
26. White A, Rose DR. Mechanism of catalysis by retaining β-glycosyl hydrolases. Curr Opin Struct Biol. 7:1997;645-651.
27. Driguez H. Thiooligosaccharides in glycobiology. Topics Curr Chem. 187:1997;85-116.
28. Notenboom V, Birsan C, Warren RAJ, Withers SG, Rose DR. Exploring the cellulose/xylan specificity of the ß-1,4-glycanase Cex from Cellulomonas fimi through crystallography and mutation. Biochemistry. 37:1998;4751-4758.
29. Klarskov K, Piens K, Stahlberg J, Hoj P, Beeumen J, Claeyssens M. Cellobiohydrolase I from Trichoderma reesei: identification of an active-site nucleophile and additional information on sequence including the glycosylation pattern of the core protein. Carbohydr Res. 304:1997;143-154.
30. Sulzenbacher G, Schülein M, Davies G. Structure of the endoglucanase I from Fusarium oxysporum: native, cellobiose, and 3,4-epoxybutyl β-D-cellobioside-inhibited forms, at 2.3 Å resolution. Biochemistry. 36:1997;5902-5911.
31. Mackenzie L, Davies G, Schülein M, Withers S. Identification of the catalytic nucleophile of endoglucanase I from Fusarium oxysporum by mass spectrometry. Biochemistry. 36:1997;5893-5901.
32. Armand S, Drouillard S, Schulein M, Henrissat B, Driguez H. A bifunctionalized fluorogenic tetrasaccharide as a substrate to study cellulases. of special interest J Biol Chem. 272:1997;2709-2713 A chemoenzymatic approach was used to synthesize a reagent that can be used as a general substrate for measuring the kinetic constants of both endoglucanases and cellobiohydrolases by resonance energy transfer.
33. Divne C, Stahlberg J, Teeri TT, Jones TA. High-resolution crystal structures reveal how a cellulose chain is bound in the 50 Å long tunnel of cellobiohydrolase I from Trichoderma reesei. of outstanding interest J Mol Biol. 275:1998;309-325 Combined data from three high-resolution structures of different catalytically deficient mutants of cellobiohydrolase I, in complex with a homologous series of cello-oligomers, afford a fantastic view of how a cellulose chain is arranged in the cellulose-binding tunnel. Ten well-defined subsites were clearly discerned and the tunnel spans a length of about 50 Å. The results are consistent with the productive binding of the cellulose chain, whereby hydrolysis would progress from the reducing towards the nonreducing end of the chain.
34. Tomme P, Warren RAJ, Miller RC, Kilburn DG, Gilkes NR. Cellulose-binding domains - classification and properties. Saddler JM, Penner MH. Enzymatic Degradation of Insoluble Polysaccharides. 1995;142-161 American Chemical Society, Washington, DC.
35. Tormo J, Lamed R, Chirino AJ, Morag E, Bayer EA, Shoham Y, Steitz TA. Crystal structure of a bacterial family-III cellulose-binding domain: a general mechanism for attachment to cellulose. EMBO J. 15:1996;5739-5751.
36. Brun E, Moriaud F, Gans P, Blackledge M, Barras F, Marion D. Solution structure of the cellulose-binding domain of the endoglucanase Z secreted by Erwinia chrysanthemi. of special interest Biochemistry. 36:1997;16074-16086 The first structure of the 62-residue family V CBD, determined by 2D NMR spectroscopy. The all-β structure exhibits an original 'ski boot' fold. Three exposed aromatic residues (Trp18, Trp43 and Tyr44) are positioned on the putative cellulose-binding face of the molecule, consistent with the planar aromatic strip of other CBDs that bind to microcrystalline cellulose. Other surface-exposed residues were suggested to play a role in the secretion of the enzyme. The structure also allowed a re-examination of the connection between this lone member of family V CBDs and segments from a variety of other bacterial proteins, notably chitinases, thereby raising the possibility that this CBD may be classified as a chitin-binding domain.
37. Jervis E, Haynes C, Kilburn D. Surface diffusion of cellulases and their isolated binding domains on cellulose. of special interest J Biol Chem. 272:1997;24016-24023 The lateral mobility on cellulose of a family II CBD, both alone and associated with its indigenous catalytic domain, was studied by fluorescent recovery after photobleaching (FRAP). Although binding to cellulose is practically irreversible, extensive lateral diffusion of the CBD takes place. The results suggest that surface diffusion is not the rate-limiting step in cellulolysis and could thus contribute significantly to the processivity of the relevant cellulases. This technique has promising potential in studying cellulase action.
38. Din N, Gilkes NR, Tekant B, Miller RCJ, Warren RAJ, Kilburn DG. Non-hydrolytic disruption of cellulose fibres by the binding domain of a bacterial cellulase. Bio/Technology. 9:1991;1096-1099.
39. Johnson P, Joshi M, Tomme P, Kilburn D, McIntosh L. Structure of the N-terminal cellulose-binding domain of Cellulomonas fimi Cen C determined by nuclear magnetic resonance spectroscopy. Biochemistry. 35:1996;14381-14394.
40. Sakon J, Irwin D, Wilson DB, Karplus PA. Structure and mechanism of endo/exocellulase E4 from Thermomonospora fusca. of outstanding interest Nat Struct Biol. 4:1997;810-818 This elegant article provides the first clear X-ray structure of a catalytic domain together with a CBD. The family 9 catalytic domain of E4 is closely linked to the family IIIc CBD and the two domains appear to interact in concert. The CBD is postulated to bind temporarily to an individual cellulose chain and to feed it into the active-site cleft of the catalytic domain. An extended cellulose chain was modeled across exposed conserved polar residues of the CBD, which align with the active-site cleft, thus suggesting the directionality of processive cleavage. Separate structures of the enzyme in complex with soluble cellodextrins led the authors to propose a structurally detailed catalytic mechanism for the family 9 cellulases. Two other novel properties are evident from the structure - E4 combines both exoglucanase and endoglucanase activities and the enzyme cleaves off cellotetraose units while functioning as an exocellulase.
41. Gal L, Gaudin C, Belaich A, Pagès S, Tardif C, Belaich J-P. CelG from Clostridium cellulolyticum: a multidomain endoglucanase acting efficiently on crystalline cellulose. of special interest J Bacteriol. 179:1997;6595-6601 Cellulase G is a cellulosomal endoglucanase from Clostridium cellulolyticum that contains a family 9 catalytic domain, a family IIIc CBD and a dockerin domain. Recombinant derivatives of this enzyme were overexpressed, including the complete enzyme, the isolated catalytic domain and the catalytic domain together with an incomplete CBD. The family IIIc CBD did not promote cellulose binding; instead, its contribution appeared to improve the activity on insoluble forms of cellulose. This work, together with the following reference by Irwin et al. [42], supports the contention that the combination of a family IIIc CBD and a family 9 catalytic domain confers the property of processivity to the hydrolysis of crystalline forms of cellulose.
42. Irwin D, Shin D-H, Zhang S, Barr BK, Sakon J, Karplus PA, Wilson DB. Roles of the catalytic domain and two cellulose binding domains of Thermomonospora fusca E4 in cellulose hydrolysis. J Bacteriol. 180:1998;1709-1714.
43. Zverlov V, Mahr S, Riedel K, Bronnenmeier K. Properties and gene structure of a bifunctional cellulolytic enzyme (CelA) from the extreme thermophile Anaerocellum thermophilum with separate glycosyl hydrolase family 9 and 48 catalytic domains. Microbiology. 144:1998;457-465.
44. Lamed R, Setter E, Kenig R, Bayer EA. The cellulosome - a discrete cell surface organelle of Clostridium thermocellum which exhibits separate antigenic, cellulose-binding and various cellulolytic activities. Biotechnol Bioeng. 13:1983;163-181.
45. Felix CR, Ljungdahl LG. The cellulosome - the exocellular organelle of Clostridium. Annu Rev Microbiol. 47:1993;791-819.
46. Bayer EA, Morag E, Lamed R. The cellulosome - a treasure-trove for biotechnology. Trends Biotechnol. 12:1994;378-386.
47. Béguin P, Lemaire M. The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation. Crit Rev Biochem Mol Biol. 31:1996;201-236.
48. Shoseyov O, Takagi M, Goldstein MA, Doi RH. Primary sequence analysis of Clostridium cellulovorans cellulose binding protein A. Proc Natl Acad Sci USA. 89:1992;3483-3487.
49. L-protein reveals an unusual degree of internal homology. Mol Microbiol. 8:1993;325-334.
50. Leibovitz E, Ohayon H, Gounon P, Béguin P. Characterization and subcellular localization of the Clostridium thermocellum scaffoldin dockerin binding protein SdbA. J Bacteriol. 179:1997;2519-2523.
51. Lemaire M, Miras I, Gounon P, Béguin P. Identification of a region responsible for binding to the cell was within the S-layer protein of Clostridium thermocellum. Microbiology. 144:1998;211-217.
52. Lamed E, Naimark J, Morgenstern E, Bayer EA. Specialized cell surface structures in cellulolytic bacteria. J Bacteriol. 169:1987;3792-3800.
53. Ahsan MM, Matsumoto M, Karita S, Kimura T, Sakka K, Ohmiya K. Purification and characterization of the family J catalytic domain derived from the Clostridium thermocellum endoglucanase CelJ. Biosci Biotechnol Biochem. 61:1997;427-431.
54. Hayashi H, Takagi KI, Fukumura M, Kimura T, Karita S, Sakka K, Ohmiya K. Sequence of xynC and properties of XynC, a major component of the Clostridium thermocellum cellulosome. J Bacteriol. 179:1997;4246-4253.
55. Kataeva I, Guglielmi G, Béguin P. Interaction between Clostridium thermocellum endoglucanase CelD and polypeptides derived from the cellulosome-integrating protein CipA: stoichiometry and cellulolytic activity of the complexes. of special interest Biochem J. 326:1997;617-624 A systematic attempt to address the question of the stoichiometry of the cohesin - dockerin interaction. Several 'mini scaffoldins', that is, constructs containing one or two cohesins with or without a CBD, were subjected to interaction with a cellulosomal dockerin-containing endoglucanase. The enzyme formed 1:1 complexes with the cohesin domain. Nevertheless, in the case of two neighboring cohesins, the binding appeared to be highly cooperative. Inclusion of a CBD was found to cause a threefold increase in the activation of cellulolysis, attributed to the targeting of the endoglucanase to the insoluble substrate.
56. Ciruela A, Gilbert HJ, Ali BRS, Hazlewood GP. Synergistic interaction of the cellulosome integrating protein (CipA) from Clostridium thermocellum with a cellulosomal endoglucanase. FEBS Lett. 422:1998;221-224.
57. Guglielmi G, Béguin P. Cellulase and hemicellulase genes of Clostridium thermocellum from five independent collections contain few overlaps and are widely scattered across the chromosome. FEMS Microbiol Lett. 161:1998;209-215.
58. Belaich J-P, Tardif C, Belaich A, Gaudin C. The cellulolytic system of Clostridium cellulolyticum. J Biotechnol. 57:1997;3-14.
59. Shimon LJW, Bayer EA, Morag E, Lamed R, Yaron S, Shoham Y, Frolow F. The crystal structure at 2.15 Å resolution of a cohesin domain of the cellulosome from Clostridium thermocellum. of outstanding interest Structure. 5:1997;381-390 This paper, together with the following article by Tavares et al. [60], describes the first known structures of cohesin domains from a cellulosomal scaffoldin subunit. The cohesin domain forms a nine-stranded β sandwich with a jelly-roll topology that is remarkably similar to the fold displayed by its neighboring family IIIa CBD. Comparative sequence homology of surface residues indicates regions of the domain that may be correlated either with dockerin binding or with other types of interactions (e.g. with adjacent domains from the same subunit or from other cellulosomal subunits).
60. Tavares GA, Béguin P, Alzari PM. The crystal structure of a type I cohesin domain at 1.7 Å resolution. J Mol Biol. 273:1997;701-713.
61. Pagés S, Belaich A, Belaich J-P, Morag E, Lamed R, Shoham Y, Bayer EA. Species-specificity of the cohesin-dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: prediction of specificity determinants of the dockerin domain. of special interest Proteins. 29:1997;517-527 Cohesin-bearing probes from two different species interact solely with dockerin-containing enzymes from the same species. The fidelity of the cohesin - dockerin interaction between these two species was correlated with sequence-alignment data in order to predict residues on the dockerin suspected of acting as 'recognition codes' for binding to the respective cohesin. The prediction awaits experimental verification by site-directed mutagenesis and/or 3D structure determination.
62. Kirby J, Martin J, Daniel A, Flint H. Dockerin-like sequences in cellulases and xylanases from the rumen cellulolytic bacterium Ruminococcus flavefaciens. FEMS Microbiol Lett. 149:1997;213-219.
63. Ohmiya K, Sakka K, Karita S, Kimura T. Structure of cellulases and their applications. Biotechnol Genet Eng Rev. 14:1997;365-414.
64. Tamaru Y, Araki T, Morishita T, Kimura T, Sakka K, Ohmiya K. Cloning, DNA sequencing, and expression of the β-1,4-mannanase gene from a marine bacterium, Vibrio sp. strain MA-138. J Ferment Bioeng. 83:1997;201-205.
65. Fanutti C, Ponyi T, Black GW, Hazlewood GP, Gilbert HJ. The conserved noncatalytic 40-residue sequence in cellulases and hemicellulases from anaerobic fungi functions as a protein docking domain. J Biol Chem. 270:1995;29314-29322.
66. Li X, Chen H, Ljungdahl L. Two cellulases, CelA and CelC, from the polycentric anaerobic fungus Orpinomyces strain PC-2 contain N-terminal docking domains for a cellulase-hemicellulase complex. Appl Environ Microbiol. 63:1997;4721-4728.