Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Cellulosomes: plant-cell-wall-degrading enzyme complexes

Key Points

  • Cellulose, the main structural component of plant cell walls, is the most abundant carbohydrate polymer in nature and is therefore a key component of the carbon cycle. Anaerobic microorganisms have evolved a system to break down plant cell wall materials, including cellulose, that involves the formation of a large extracellular enzyme complex called the cellulosome.

  • Although anaerobic fungi as well as anaerobic bacteria are believed to produce cellulosomes, so far full genetic evidence for their presence has only been obtained in anaerobic bacteria. To date, cellulosomes have been identified in 12 different bacterial species, and this list is expected to continue growing.

  • Cellulosomes comprise a fibrillar protein known as the scaffolding protein or scaffoldin with cellulosomal enzyme subunits positioned periodically along the fibrils. Typically, the scaffoldin contains enzyme-binding sites known as cohesins, and a cellulose-binding domain (CBD) or carbohydrate-binding module (CBM). The enzyme subunits bind to the cohesins via cohesin-binding sites known as dockerins. The properties of the scaffoldins vary between species. Additionally, cellulosomes can contain either one or several different scaffoldins that can bind different combination of enzymes. This variation and the presence of many cellulosomal enzymes means that any single microorganism can secrete a variety of cellulosomes with many different compositions. The cellulosomal enzymes include cellulases, hemicellulases, pectinase, chitinase and many ancillary enzymes that can degrade plant cell wall materials.

  • In biotechnology, there is great interest in exploiting the properties of cellulosomes. 'Mini-cellulosomes' can be created, which, because they contain specific cohesins, will only bind to specific enzymes. These constructs have been used to great effect in cellulosome research in the study of the synergistic effects of cellulosomal enzymes and the cohesin–dockerin interaction, for example, but it is also hoped that mini-cellulosome constructs could be used in the future to develop artificial metabolic pathways that allow the synthesis of any desired product. There is also great interest in the heterologous expression of cellulosome genes, such that non-cellulose degrading organisms can be converted to cellulose degraders.

Abstract

Cellulose, the main structural component of plant cell walls, is the most abundant carbohydrate polymer in nature. Although abundant, it is extremely difficult to degrade, as it is insoluble and is present as hydrogen-bonded crystalline fibres. Anaerobic microorganisms have evolved a system to break down plant cell walls that involves the formation of a large extracellular enzyme complex called the cellulosome, which consists of a scaffolding protein and many bound cellulases. Cellulosomes have many potential biotechnological applications as the conversion of cellulosic biomass into sugars by cellulosomes could result in the production of high-value products such as ethanol or organic acids from inexpensive renewable resources. Rapid advances in cellulosome research are providing basic information for the development of both in vitro and in vivo systems to achieve such goals.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: A schematic model of a Clostridium cellulovorans cellulosome.
Figure 2: The modular structure of scaffoldins from various microorganisms.
Figure 3: A model of the Acetivibrio cellulolyticus cellulosome.
Figure 4: A model of a designer mini-cellulosome.

Similar content being viewed by others

References

  1. Mansfield, S. D., Mooney, C. & Saddler, J. N. Substrate and enzyme characteristics that limit cellulose hydrolysis. Biotechnol. Prog. 15, 804–816 (1999).

    Article  CAS  PubMed  Google Scholar 

  2. Lynd, L. R., Weimer, P. J., van Zyl, W. H. & Pretorius, I. S. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 66, 506–577 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Warren, R. A. J. Microbial hydrolysis of polysaccharides. Annu. Rev. Microbiol. 50, 183–212 (1996).

    Article  CAS  PubMed  Google Scholar 

  4. Bayer, E. A., Setter, E. & Lamed, R. Organization and distribution of the cellulosome in Clostridium thermocellum. J. Bacteriol. 163, 552–559 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Bayer, E. A., Belaich, J. -P., Shoham, Y. & Lamed, R. The cellulosomes: multi-enzyme machines for degradation of plant cell wall polysaccharides. Annu. Rev. Microbiol. (in the press).

  6. Bayer, E. A., Morag, E. & Lamed, R. The cellulosome — a treasure trove for biotechnology. Trends Biotechnol. 12, 378–386 (1994).

    Article  Google Scholar 

  7. Bayer, E. A., Shimon, L. J. W., Shoham, Y. & Lamed, R. Cellulosomes — structure and ultrastructure. J. Struct. Biol. 124, 221–234 (1998).

    Article  CAS  PubMed  Google Scholar 

  8. Bayer, E. A., Shoham, Y. & Lamed, R. Cellulose-decomposing prokaryotes and their enzyme systems. in The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community (eds Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. & Stackebrandt, E.) 3rd edition <http://141.150.157.117:8080/prokPUB/chaprender/jsp/showchap.jsp?chapnum=297&initsec=01_00> (Springer–Verlag, New York, 2000).

    Google Scholar 

  9. Beguin, P. & Alzari, P. M. The cellulosome of Clostridium thermocellum. Biochem. Soc. Trans. 26, 178–185 (1998).

    Article  CAS  PubMed  Google Scholar 

  10. Doi, R. H., Kosugi, A., Murashima, K., Tamaru, Y. & Han, S. O. Cellulosomes from mesophilic bacteria. J. Bacteriol. 185, 5907–5914 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ohmiya, K., Sakka, K., Kimura, T. & Morimoto, K. Application of microbial genes to recalcitrant biomass utilization and environmental conservation. J. Biosci. Bioeng. 95, 549–561 (2003).

    Article  CAS  PubMed  Google Scholar 

  12. Schwarz, W. H. The cellulosome and cellulose degradation by anaerobic bacteria. Appl. Microbiol. Biotechnol. 56, 634–649 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Wilson, C. A. & Wood, T. M. The anaerobic fungus Neocallimastix frontalis: isolation and properties of a cellulosome-type enzyme fraction with the capacity to solubilize hydrogen-bond-ordered cellulose. Appl. Microbiol. Biotechnol. 37, 125–129 (1992).

    Article  CAS  Google Scholar 

  14. Ali, B. R. S. et al. Cellulases and hemicellulases of the anaerobic fungus Piromyces constitute a multiprotein cellulose-binding complex and encoded by multigene families. FEMS Microbiol. Lett. 125, 15–22 (1995).

    Article  CAS  PubMed  Google Scholar 

  15. Fanutti, C., Ponyi, T., Black, G. W., Hazelwood, G. P. & Gilbert, H. J. The conserved noncatalytic 40-residue sequence in cellulases and hemicellulases from anaerobic fungi functions as a protein docking domain. J. Biol. Chem. 270, 29314–29322 (1995).

    Article  CAS  PubMed  Google Scholar 

  16. Fillingham, I. J., Kroon, P. A., Williamson, G., Gilbert, H. J. & Hazlewood, G. P. A modular cinnamoyl ester hydrolase from the anaerobic fungus Piromyces equi acts synergistically with xylanase and is part of a multiprotein cellulose-binding cellulase–hemicellulase complex. Biochem. J. 343, 215–224 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Steenbakkers, P. J. M. et al. Non-catalytic docking domains of cellulosomes of anaerobic fungi. J. Bacteriol. 183, 5325–5333 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Steenbakkers, P. J. M. et al. The β-glucosidase in the cellulosome of the anaerobic fungus Piromyces sp. strain E2 is a family 3 glycoside hydrolase. Biochem. J. 370, 963–970 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sabathe, F., Belaich, A. & Soucaille, P. Characterization of the cellulolytic complex (cellulosome) of Clostridium acetobutylicum. FEMS Microbiol. Lett. 217, 15–22 (2002).

    Article  CAS  PubMed  Google Scholar 

  20. Lee, S. F., Forsberg, C. W. & Gibbins, L. N. Cellulolytic activity of Clostridium acetobutylicum. Appl. Environ. Microbiol. 50, 220–228 (1985).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Madkour, M. & Mayer, F. Structural organization of the intact bacterial cellulosome as revealed by electron microscopy. Cell Biol. Int. 27, 831–836 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Xu, Q. et al. The cellulosome system of Acetivibrio cellulolyticus includes a novel type of adaptor protein and a cell surface anchoring protein. J. Bacteriol. 185, 4548–4557 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pohlschroder, M. D., Leschine, S. B. & Canale-Parola, E. Multicomplex cellulase–xylanase system of Clostridium papyrosolvens C7. J. Bacteriol. 176, 70–76 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Pohlschroder, M., Canale-Parola, E. & Leschine, S. B. Ultrastructural diversity of the cellulase complexes of Clostridium papyrosolvens C7. J. Bacteriol. 177, 6625–6629 (1995). One of the best structural studies showing the subpopulations of cellulosomes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ali, B. R. S., Romaniec, M. P. M., Hazlewood, G. P. & Freedman, R. B. Characterization of the subunits in an apparently homogeneous subpopulation of Clostridium thermocellum cellulosomes. Enzyme Microb. Technol. 17, 705–711 (1995).

    Article  CAS  PubMed  Google Scholar 

  26. Murashima, K., Kosugi, A. & Doi, R. H. Determination of subunit composition of Clostridium cellulovorans cellulosomes that degrade plant cell walls. Appl. Environ. Microbiol. 68, 1610–1615 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Park, J. -S., Matano, Y. & Doi, R. H. Cohesin–dockerin interactions of cellusomal subunits of Clostridium cellulovorans. J. Bacteriol. 183, 5431–5435 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Boraston, A. B. et al. in Carbohydrate Bioengineering (eds Gilbert, H. J., Davies, G. J., Henrissat, B. & Svensson, B.) 202–211 (The Royal Society of Chemistry, Cambridge, 1999).

    Google Scholar 

  29. Leibovitz, E. & Beguin, P. A new type of cohesin domain that specifically binds the dockerin domain of the Clostridium thermocellum cellulosome integrating protein CipA. J. Bacteriol. 178, 3077–3084 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Shoseyov, O., Takagi, M., Goldstein, M. & Doi, R. H. Primary sequence analysis of Clostridium cellulovorans cellulose binding protein A (CbpA). Proc. Natl Acad. Sci. USA 89, 3483–3487 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Pages, S. et al. Sequence analysis of scaffolding protein CipC and ORFXp, a new cohesin-containing protein in Clostridium cellulolyticum: comparison of various cohesin domains and subcellular localization of ORFXp. J. Bacteriol. 181, 1801–1810 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Gerngross, U., Romaniec, M. P. M., Kobayashi, T., Huskisson, N. S. & Demain, A. L. Sequencing of a Clostridium thermocellum gene (cipA) encoding the cellulosomal SL-protein reveals an unusual degree of internal homology. Mol. Microbiol. 8, 325–334 (1993).

    Article  CAS  PubMed  Google Scholar 

  33. Kakiuchi, M. et al. Cloning and DNA sequencing of the genes encoding Clostridium josui scaffolding protein CipA and cellulase CelD and identification of their gene products as major components of the cellulosome. J. Bacteriol. 180, 4303–4308 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Ding, S. -Y., Bayer, E. A., Steiner, D., Shoham, Y. & Lamed, R. A novel cellulosomal scaffoldin from Acetivibrio cellulolyticus that contains a family-9 glycosyl hydrolase. J. Bacteriol. 181, 6720–6729 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Ding, S. -Y. et al. Cellulosomal scaffoldin-like proteins from Ruminococcus flavefaciens. J. Bacteriol. 183, 1945–1953 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Lemaire, M., Ohayon, H., Gounon, P., Fujino, T. & Beguin, P. OlpB, a new outer layer protein of Clostridium thermocellum, and binding of its S-layer-like domains to components of the cell envelope. J. Bacteriol. 177, 2451–2459 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Rincon, M. T. et al. Novel organization and divergent dockerin specificities in the cellulosome system of Ruminococcus flavefaciens. J. Bacteriol. 185, 703–713 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tokatlidis, K., Salamitou, S., Beguin, P., Dhurjati, P. & Aubert, J. -P. Interaction of the duplicated segment carried by Clostridium thermocellum cellulases with cellulosome components. FEBS Lett. 291, 185–188 (1991). An early example of a dockerin–cohesin interaction.

    Article  CAS  PubMed  Google Scholar 

  39. Pages, S. et al. Species-specificity of the cohesin–dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: prediction of specificity determinants of the dockerin domain. Proteins: Struct. Funct. Genet. 29, 517–527 (1997). An important illustration of the species-specificity of the cohesin–dockerin interaction.

    Article  CAS  Google Scholar 

  40. Miras, I., Schaeffer, F., Beguin, P. & Alzari, P. M. Mapping by site-directed mutagenesis of the region responsible for cohesin–dockerin interaction on the surface of the seventh cohesin domain of Clostridium thermocellum CipA. Biochemistry 41, 2115–2119 (2002).

    Article  CAS  PubMed  Google Scholar 

  41. Schaeffer, F. et al. 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 41, 2106–2114 (2002).

    Article  CAS  PubMed  Google Scholar 

  42. Shimon, L. J. et al. A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly. Structure 5, 381–390 (1997).

    Article  CAS  PubMed  Google Scholar 

  43. Mechaly, A. S. et al. Cohesin–dockerin recognition in cellulosome assembly: experiment versus hypothesis. Proteins 39, 170–177 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Tavares, G. A., Beguin, P. & Alzari, P. M. The crystal structure of a Type I cohesin domain at 1. 7 Å resolution. J. Mol. Biol. 273, 701–713 (1997).

    Article  CAS  PubMed  Google Scholar 

  45. Spinelli, S. et al. Crystal structure of a cohesin module from Clostridium cellulolyticum: Implications for dockerin recognition. J. Mol. Biol. 304, 189–200 (2000).

    Article  CAS  PubMed  Google Scholar 

  46. Carvalho, A. L. et al. Cellulosome assembly revealed by the crystal structure of the cohesin–dockerin complex. Proc. Natl Acad. Sci. USA 100, 13809–13814 (2003). A structural analysis of the interaction between cohesins and dockerins.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Gaudin, C., Belaich, A., Champ, S. & Belaich, J. -P. CelE, a multidomain cellulase from Clostridium cellulolyticum: a key enzyme in the cellulosome? J. Bacteriol. 182, 1910–1915 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Tamaru, Y., Karita, S., Ibrahim, A., Chan, H. & Doi, R. H. A large gene cluster for the Clostridium cellulovorans cellulosome. J. Bacteriol. 182, 5906–5910 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Nolling, J. et al. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183, 4823–4838 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Belaich, A. et al. Cel9M, a new family 9 cellulase of the Clostridium cellulolyticum cellulosome. J. Bacteriol. 184, 1378–1384 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Guglielmi, G. & Beguin, 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, 209–215 (1998).

    Article  CAS  PubMed  Google Scholar 

  52. Fujino, T., Beguin, P. & Aubert, J. -P. Organization of a Clostridium thermocellum gene cluster encoding the cellulosomal scaffolding protein CipA and a protein possibly involved in attachment of the cellulosome to the cell surface. J. Bacteriol. 175, 1891–1899 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lamed, R., Setter, E. & Bayer, E. A. Characterization of a cellulose-binding cellulase-containing complex in Clostridium thermocellum. J. Bacteriol. 156, 828–836 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Blair, B. G. & Anderson, K. L. Regulation of cellulose-inducible structures of Clostridium cellulovorans. Can. J. Microbiol. 45, 242–249 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Attwood, G. T., Blaschek, H. P. & White, B. A. Transcriptional analysis of the Clostridium cellulovorans endoglucanase gene, engB. FEMS Microbiol. Lett. 124, 277–284 (1994).

    Article  CAS  PubMed  Google Scholar 

  56. Han, S. O., Yukawa, H., Inui, M. & Doi, R. H. Regulation of expression of cellulosomal cellulase and hemicellulase genes in Clostridium cellulovorans. J. Bacteriol. 185, 6067–6075 (2003). Illustration of the coordinate expression of cellulase genes and its regulation by a catabolite-repression-like mechanism.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ali, B. R. S., Romaniec, M. P. M., Hazlewood, G. P. & Freedman, R. B. Characterization of the subunits in an apparently homogeneous subpopulation of Clostridium thermocellum cellulosomes. Enzyme Microb. Technol. 17, 705–711 (1995).

    Article  CAS  PubMed  Google Scholar 

  58. Han, S. O., Yukawa, H., Inui, M. & Doi, R. H. Transcription of Clostridium cellulovorans cellulosomal cellulase and hemicellulase genes. J. Bacteriol. 185, 2520–2527 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mishra, S., Beguin, P. & Aubert, J. P. Transcription of Clostridium thermocellum endoglucanase genes celF and celD. J. Bacteriol. 173, 80–85 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dror, T. W. et al. Regulation of the cellulosomal celS (cel48A) gene of Clostridium thermocellum is growth rate dependent. J. Bacteriol. 185, 3042–3048 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Dror, T. W., Rolider, A., Bayer, E. A., Lamed, R. & Shoham, Y. Regulation of expression of scaffoldin-related genes in Clostridium thermocellum. J. Bacteriol. 185, 5109–5116 (2003). References 60 and 61 show that the expression of cellulosomal genes is growth-rate-dependent.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Jennert, K. C. B., Tardif, C., Young, D. I. & Young, M. Gene transfer to Clostridium cellulolyticum ATCC 35319. Microbiology 12, 3071–3080 (2000).

    Article  Google Scholar 

  63. Tardif, C., Maamar, H., Balfin, M. & Belaich, J. P. Electrotransformation studies in Clostridium cellulolyticum. J. Ind. Microbiol. Biotechnol. 27, 271–274 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. Tyurin, M. V., Desai, S. G. & Lynd, L. R. Electrotransformation of Clostridium thermocellum. Appl. Environ. Microbiol. 70, 883–890 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Perret, S., Maamar, H., Belaich, J. P. & Tardif, C. Use of antisense RNA to modify the composition of cellulosomes produced by Clostridium cellulolyticum. Mol. Microbiol. 51, 599–607 (2004). Anti-sense RNA technology was used to illustrate the importance of exoglucanase Cel48F in the full expression of cellulosome activity.

    Article  CAS  PubMed  Google Scholar 

  66. Maamar, H. et al. Cellulolysis is severely affected in Clostridium cellulolyticum strain cipCMut1. Mol. Microbiol. 51, 589–598 (2004). Shows the importance of the expression of the scaffoldin gene in the expression of downstream genes of cipC and the enzymes in the cipC gene cluster for full expression of the cellulosome activity.

    Article  CAS  PubMed  Google Scholar 

  67. Mechaly, A. et al. Cohesin–dockerin interaction in cellulosome assembly. J. Biol. Chem. 276, 9883–9888 (2001).

    Article  CAS  PubMed  Google Scholar 

  68. Fierobe, H. -P. et al. Design and production of active cellulosome chimeras: selective incorporation of dockerin-containing enzymes into defined functional complexes. J. Biol. Chem. 276, 21257–21261 (2001).

    Article  CAS  PubMed  Google Scholar 

  69. Fierobe, H. -P. et al. Degradation of cellulose substrates by cellulosome chimeras. J. Biol. Chem. 277, 49621–49630 (2002). A good example of the use of chimeric mini-scaffoldins to analyse the functions of enzymes, CBDs and activity.

    Article  CAS  PubMed  Google Scholar 

  70. Murashima, K., Kosugi, A. & Doi, R. H. Synergistic effects on crystalline cellulose degradation between cellulosomal cellulases from Clostridium cellulovorans. J. Bacteriol. 184, 5088–5095 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kataeva, I., Guglielmi, G. & Beguin, P. Interaction between Clostridium thermocellum endoglucanase CelD and polypeptides derived from the cellulosome-integrating protein CipA: stoichiometry and cellulolytic activity of the complexes. Biochem. J. 326, 617–624 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Murashima, K., Kosugi, A. & Doi, R. H. Synergistic effects of cellulosomal xylanase and cellulases from Clostridium cellulovorans on plant cell wall degradation. J. Bacteriol. 85, 1518–1524 (2003).

    Article  CAS  Google Scholar 

  73. Kosugi, A., Murashima, K. & Doi, R. H. Characterization of non-cellulosomal subunits, ArfA and BgaA from Clostridium cellulovorans, that cooperate with the cellulosome in plant cell wall degradation. J. Bacteriol. 184, 6859–6865 (2002). Evidence for interactions between the cellulosome and non-cellulosomal enzymes.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Morag, E., Bayer, E. A. & Lamed, R. Relationship of cellulosomal and noncellulosomal xylanases of Clostridium thermocellum to cellulose-degrading enzymes. J. Bacteriol. 172, 6098–6105 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Levy, I. & Shoseyov, O. Cellulose-binding domains: biotechnological applications. Biotechnol. Adv. 20, 191–213 (2002). Describes the practical applications of CBD technology.

    Article  CAS  PubMed  Google Scholar 

  76. Tomme, P. et al. Characterization and affinity applications of cellulose-binding domains. J. Chromatogr. B Biomed. Sci. Appl. 715, 283–296 (1998).

    Article  CAS  PubMed  Google Scholar 

  77. Shpigel, E. et al. Immobilization of recombinant heparinase I fused to cellulose binding domain. Biotechnol. Bioeng. 65, 17–23 (1999).

    Article  CAS  PubMed  Google Scholar 

  78. Shpigel, E., Roiz, L., Goren, R. & Shoseyov, O. Bacterial cellulose binding domain modulates in vitro elongation of different plant cells. Plant Physiol. 117, 1185–1194 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Shoseyov, O., Levy, I., Shani, Z. & Mansfield, S. D. Modulation of wood fibers and paper by cellulose binding domains. in Applications of Enzymes to Lignocellulosics (eds Mansfield, S. D. & Saddler, J. N.) 116–131 (American Chemical Society, Washington DC, 2003).

    Chapter  Google Scholar 

  80. Shpigel, E., Elias, D., Cohen, I. R. & Shoseyov, O. Production and purification of a recombinant human hsp60 eptiope using the cellulose-binding domain in Escherichia coli. Protein Expr. Purif. 14, 185–191 (1998).

    Article  CAS  PubMed  Google Scholar 

  81. Perret, S. et al. Production of heterologous and chimeric scaffoldins by Clostridium acetobutylicum ATCC 824. J. Bacteriol. 186, 253–257 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sabathe, F. & Soucaille, P. Characterization of the CipA scaffolding protein and in vivo production of a minicellulosome in Clostridium acetobutylicum. J. Bacteriol. 185, 1092–1096 (2003). References 81 and 82 show the potential for converting C. acetobutylicum to a cellulose degrader.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Kim, A. Y., Attwood., G. T., Holt, S. M., White, B. A. & Blaschek, H. P. Heterologous expression of endo-β-1,4-D-glucanase from Clostridium cellulovorans in Clostridium acetobutylicum ATCC 824 following transformation of the engB gene. Appl. Environ. Microbiol. 60, 337–340 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Murashima, K., Kosugi, A. & Doi, R. H. Thermostabilization of cellulosomal endoglucanase EngB from Clostridium cellulovorans by in vitro DNA recombination with non-cellulosomal endoglucanase EngD. Mol. Microbiol. 45, 617–626 (2002). The DNA-shuffling technique was used to form a more heat-stable endoglucanase from two mesophilic enzymes.

    Article  CAS  PubMed  Google Scholar 

  85. Murashima, K. & Doi, R. H. Selection of heat stable Clostridium cellulovorans cellulases after in vitro recombination. Methods in Molecular Biology Series 230, 231–237 (eds Arnold, F. H. & Georgiou, G.) (Humana Press, Totowa, New Jersey, USA, 2003).

    Google Scholar 

  86. Ding, S. -Y., Bayer, E. A., Steiner, D., Shoham, Y. & Lamed, R. A scaffoldin of the Bacteroides cellulosolvens cellulosome that contains 11 type II cohesins. J. Bacteriol. 182, 4915–4925 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Berger, E., Jones, W. A., Jones, D. T. & Woods, D. R. Sequencing and expression of a cellodextrinase (ced1) gene from Butyrivibrio fibrisolvens H17c cloned in Escherichia coli. Mol. Gen. Genet. 223, 310–318 (1990).

    Article  CAS  PubMed  Google Scholar 

  88. Lamed, R., Naimark, J., Morgenstern, E. & Bayer, E. A. Specialized surface structure in cellulolytic bacteria. J. Bacteriol. 169, 3792–3800 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Sleat, R., Mah, R. A. & Robinson, R. Isolation and characterization of an anaerobic, cellulolytic bacterium, Clostridium cellulovorans sp. nov. Appl. Environ. Microbiol. 8, 88–91 (1984).

    Google Scholar 

  90. Ohara, H., Karita, S., Kimura, T., Sakka, K. & Ohmiya, K. Characterization of the cellulolytic complex (cellulosome) from Ruminococcus albus. Biosci. Biotechnol. Biochem. 64, 254–260 (2000).

    Article  CAS  PubMed  Google Scholar 

  91. Dalrymple, B. P. et al. Three Neocallimastix patriciarum esterases associated with the degradation complex polysaccharides are members of a new family of hydrolases. Microbiology 143, 2605–2614 (1997).

    Article  CAS  PubMed  Google Scholar 

  92. Qiu, X., Selinger, B., Yanke, L. -J. & Cheng, K. -J. Isolation and analysis of two cellulase cDNAs from Orpinomyces joyonii. Gene 245, 119–126 (2000).

    Article  CAS  PubMed  Google Scholar 

  93. Borneman, W. S., Akin, D. E. & Ljungdahl, L. G. Fermentation products and plant cell wall degrading enzymes produced by monocentric and polycentric anaerobic ruminal fungi. Appl. Environ. Microbiol. 55, 1066–1073 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Teunissen, M. J., Op den Camp, H. J. M., Orpin, C. G., Huis in't Veld, J. H. J. & Vogels, G. D. Comparison of growth characteristics of anaerobic fungi isolated from ruminant and non-ruminant herbivores during cultivation in a defined medium. J. Gen. Microbiol. 137, 1401–1408 (1991).

    Article  CAS  PubMed  Google Scholar 

  95. Xu, Q. et al. Architecture of the Bacteroides cellulosolvens cellulosome: description of a cell surface-anchoring scaffoldin and a family 48 cellulase. J. Bacteriol. 186, 968–977 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The research reported from our laboratory was supported in part by a grant from the US Department of Energy.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roy H. Doi.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

DATABASES

Entrez

Clostridium acetobutylicum

Clostridium thermocellum

SwissProt

CipA

FURTHER INFORMATION

Roy Doi's laboratory

Glossary

CELLULOSE

The most abundant plant polysaccharide consisting of (1→4)β-D-glucan chains hydrogen-bonded to one another along their length.

HEMICELLULOSE

Cross-linking glycans that comprise up to about 30% of plant cell walls; the two major hemicelluloses are xyloglucans and glucuronoarabinoxylans.

CELLULOSOME

An extracellular enzyme complex consisting of a scaffoldin and cellulosomal enzymes that are capable of degrading plant cell walls. Cellulosomes are produced by anaerobic microorganisms.

CELLULASE

Glycosyl hydrolases that degrade cellulose.

SCAFFOLDIN

A scaffolding protein found in cellulosomes containing cohesin domains that bind cellulosomal enzymes.

COHESIN

Domains in the scaffoldin to which cellulosomal enzymes are bound. There are at least three types of cohesins, which vary in amino acid sequence.

DOCKERIN

Duplicated sequences present in cellulosomal enzymes that bind to cohesins. There are at least three types of dockerins, which vary in amino acid sequence.

AVICEL

A commercially available microcrystalline cellulose.

CELLOBIOSE

An individual unit of cellulose.

SIGMA-A

Sigma factors are variable protein components of the bacterial RNA polymerase that influence transcription by determining where the polymerase binds to DNA. In Bacillus, σA is a housekeeping sigma factor, σB an alternative sigma factor that responds to stress and σL the Bacillus subtilis homologue of σ54, the major variant sigma factor in E. coli.

CATABOLITE REPRESSION

Transcriptional repression of a prokaryotic operon by the metabolic products of the enzymes that are encoded by the operon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Doi, R., Kosugi, A. Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat Rev Microbiol 2, 541–551 (2004). https://doi.org/10.1038/nrmicro925

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro925

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing