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Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides

Nature Reviews Microbiology volume 15, pages 83–95 (2017)Cite this article

Subjects

Key Points

  • Cellulosomes are self-assembled multienzyme complexes that are highly efficient at degrading lignocellulose, mainly owing to common substrate targeting and consequent enzyme proximity that, together, generate substrate channelling and synergistic action.

  • Cellulosomes have been identified in several anaerobic bacteria, with each species presenting its own molecular arrangement with varying degrees of complexity.

  • The prevalence of cellulosomes as rare but central components in various ecosystems reflects the benefits of this enzymatic strategy.

  • The cohesin–dockerin interaction has been studied extensively and is one of the strongest non-covalent interactions known in nature.

  • The composition of cellulosomes is regulated and varied by the nature of the growth substrate (carbon source) of the parent bacterium.

  • The cellulosome, as one of the most efficient machineries for the degradation of plant cell walls, can potentially be used for the large-scale conversion of biomass.

  • Owing to the modular nature of cellulosomes, cellulosomal components have been proposed for use in additional biotechnological applications, notably, together with other affinity systems.

Abstract

Cellulosomes are multienzyme complexes that are produced by anaerobic cellulolytic bacteria for the degradation of lignocellulosic biomass. They comprise a complex of scaffoldin, which is the structural subunit, and various enzymatic subunits. The intersubunit interactions in these multienzyme complexes are mediated by cohesin and dockerin modules. Cellulosome-producing bacteria have been isolated from a large variety of environments, which reflects their prevalence and the importance of this microbial enzymatic strategy. In a given species, cellulosomes exhibit intrinsic heterogeneity, and between species there is a broad diversity in the composition and configuration of cellulosomes. With the development of modern technologies, such as genomics and proteomics, the full protein content of cellulosomes and their expression levels can now be assessed and the regulatory mechanisms identified. Owing to their highly efficient organization and hydrolytic activity, cellulosomes hold immense potential for application in the degradation of biomass and are the focus of much effort to engineer an ideal microorganism for the conversion of lignocellulose to valuable products, such as biofuels.

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Figure 1: Types of cellulosome system.
Figure 2: Alternative roles of adaptor scaffoldins.
Figure 3: Crystal structure of a Clostridium thermocellum cellulosome fragment.
Figure 4: State-of-the-art designer cellulosome technology.

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Acknowledgements

The authors are grateful for long-term collaborations with R. Lamed (co-discoverer of the cellulosome concept), M. Wilchek, E. Morag, Y.l Shoham, I. Borovok, I. Mizrahi, Y. Barak, the late F. Frolow, O. Livnah, S. P. Smith, D. Wilson, M. Himmel, S.-Y. Ding, Y. Bomble, H. Flint, B. White, J.-P. Belaich, A. Belaich, H.-P. Fierobe, B. Henrissat, M. Carrion-Vazquez, M. Czjzek, S. Jindou, M. Morrison, H. Gilbert, C. Fontes, H. Gaub, M. Nash, R. Bernardi, K. Schulten, and the many superb students, technicians and postdoctoral fellows who have contributed to the described research throughout the years. The authors specifically thank J. Weinstein for the design and preparation of figure 3 and B. Dassa for pre-publication of bioinformatic data. E.A.B. is currently supported by the following funding agencies: the Israel Science Foundation (ISF; grant 1349); the Israeli Center of Research Excellence (I-CORE Center; grant 152/11) managed by the ISF; by the United States–Israel Binational Science Foundation (BSF), Jerusalem, Israel; the European Union, Area NMP.2013.1.1-2: Self-assembly of naturally occurring nanosystems: CellulosomePlus Project number 604530; and European Union Horizon 2020 contract: Sustainable production of next generation biofuels from waste streams: WASTE2FUELS. The authors also acknowledge the Dana and Yossie Hollander Center for Structural Proteomics, the Leona M. and Harry B. Helmsley Charitable Trust, the Brazilian Friends of the Weizmann Institute of Science and the Jewish Community Endowment Fund. E.A.B. is the incumbent of The Maynard I. and Elaine Wishner Chair of Bio-organic Chemistry.

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  1. Department of Biomolecular Sciences, The Weizmann Institute of Science, 234 Herzl Street, 7610001, Rehovot, Israel

    Lior Artzi, Edward A. Bayer & Sarah Moraïs

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Glossary

Cellulose

A crystalline polysaccharide comprising very long, linear, unbranched chains of pure glucose (up to 15,000 units) that are connected by β-1,4-linkages and are resistant to simple enzymatic hydrolysis.

Hemicellulose

A mixture of branched polysaccharides that are relatively easily hydrolysable. Hemicelluloses include, among other polysaccharides, xylans, xyloglucans, glucuronoxylans, arabinoxylans, arabinans, mannans, glucomannans and β-glucans.

Lignin

A complex organic polymer that consists of various crosslinked aromatic alcohols. Lignin can be covalently linked to hemicellulose by ferulic acid side chains. Lignin confers structural support and turgidity to the plant cell wall.

Lignocellulose

A general term that refers to the composite of cellulose, hemicellulose, pectin and lignin, and indicates the plant cell wall and biomass.

Modules

Independently folding portions of proteins that have independent functions.

Thermophile

A bacterium or fungus that lives in an environment with relatively high temperatures. The optimum temperature for the growth of thermophiles is usually between 45 °C and 70 °C. Hyperthermophilic microorganisms thrive at temperatures that exceed 70 °C.

Mesophiles

Bacteria and fungi that live at moderate temperatures. The optimum temperature for the growth of mesophiles is usually between 20 °C and 45 °C.

Glycoside hydrolases

Enzymes that hydrolyse the glycosidic linkage between two carbohydrates or between a carbohydrate and a non-carbohydrate group.

Cellulases

A group of enzymes that catalyse cleavage of the cellulose chain.

Carbohydrate esterases

Enzymes that deacetylate substituted saccharides or alkyl (for example, ethyl) groups of hemicelluloses.

Polysaccharide lyases

Enzymes that cleave polysaccharide chains that contain uronic acid.

Exoglucanase

A cellulase that hydrolyses the cellulose chain only at one of its free termini (reducing or non-reducing) and then degrades the substrate in a processive manner.

Endoglucanase

A cellulase that can hydrolyse the glycosidic bond at any site along a cellulose chain.

β-Glucosidases

Cellulases that hydrolyse only terminal, non-reducing glucose units from short cellodextrins.

Carbon catabolite repression

A regulatory mechanism that, in the presence of a preferred substrate, prevents the expression of genes that are required for the utilization of secondary sources of carbon.

Two-component system

A signal transduction pathway that involves a sensor in the extracellular environment and an intracellular response regulator.

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Artzi, L., Bayer, E. & Moraïs, S. Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat Rev Microbiol 15, 83–95 (2017). https://doi.org/10.1038/nrmicro.2016.164

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