Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components

Adams, J; Currie, M; Ali, S; Bayer, E; Jia, Z; Smith, S

Title: Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components

Full Record
Other Related Research

Abstract

Cellulosomes are large, multienzyme, plant cell wall-degrading protein complexes found affixed to the surface of a variety of anaerobic microbes. The core of the cellulosome is a noncatalytic scaffoldin protein, which contains several type-I cohesin modules that bind type-I dockerin-containing enzymatic subunits, a cellulose-binding module, an X module, and a type-II dockerin that interacts with type-II cohesin-containing cell surface proteins. The unique arrangement of the enzymatic subunits in the cellulosome complex, made possible by the scaffoldin subunit, promotes enhanced substrate degradation relative to the enzymes free in solution. Despite representative high-resolution structures of all of the individual modules of the cellulosome, this mechanism of enzymatic synergy remains poorly understood. Consequently, a model of the entire cellulosome and a detailed picture of intermodular contacts will provide more detailed insight into cellulosome activity. Toward this goal, we have solved the structure of a multimodular heterodimeric complex from Clostridium thermocellum composed of the type-II cohesin module of the cell surface protein SdbA bound to a trimodular C-terminal fragment of the scaffoldin subunit CipA to a resolution of 1.95 {angstrom}. The linker that connects the ninth type-I cohesin module and the X module has elevated temperature factors, reflecting an inherent flexibility within this region.more »« less

Authors:: Adams, J; Currie, M; Ali, S; Bayer, E; Jia, Z; Smith, S

Publication Date:: Sat Dec 31 00:00:00 EST 2011

Research Org.:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Org.:: USDOE SC OFFICE OF SCIENCE (SC)

OSTI Identifier:: 1041878

Report Number(s):: BNL-97556-2012-JA
Journal ID: ISSN 0022-2836; JMOBAK; TRN: US201212%%289

DOE Contract Number:: DE-AC02-98CH10886

Resource Type:: Journal Article

Journal Name:: Journal of Molecular Biology

Additional Journal Information:: Journal Volume: 396; Journal Issue: 4; Journal ID: ISSN 0022-2836

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; CLOSTRIDIUM THERMOCELLUM; CRYSTAL STRUCTURE; DIMERIZATION; DIMERS; ENZYMES; FLEXIBILITY; PLANT CELLS; PROTEINS; RESOLUTION; SEDIMENTATION; SUBSTRATES; SYMMETRY; VELOCITY

Citation Formats


                    Adams, J, Currie, M, Ali, S, Bayer, E, Jia, Z, and Smith, S. Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components.  United States: N. p., 2011. 
        Web.

Copy to clipboard


                    Adams, J, Currie, M, Ali, S, Bayer, E, Jia, Z, & Smith, S. Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components.  United States.

Copy to clipboard


                    Adams, J, Currie, M, Ali, S, Bayer, E, Jia, Z, and Smith, S. 2011.  
        "Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components".  United States.

Copy to clipboard


                    
@article{osti_1041878,

  title        = {Insights into Higher-Order Organization of the Cellulosome Revealed by a Dissect-and build Approach: Crystal Structure of Interacting Clostridium thermocellum Multimodular components},

  author       = {Adams, J and Currie, M and Ali, S and Bayer, E and Jia, Z and Smith, S},

  abstractNote = {Cellulosomes are large, multienzyme, plant cell wall-degrading protein complexes found affixed to the surface of a variety of anaerobic microbes. The core of the cellulosome is a noncatalytic scaffoldin protein, which contains several type-I cohesin modules that bind type-I dockerin-containing enzymatic subunits, a cellulose-binding module, an X module, and a type-II dockerin that interacts with type-II cohesin-containing cell surface proteins. The unique arrangement of the enzymatic subunits in the cellulosome complex, made possible by the scaffoldin subunit, promotes enhanced substrate degradation relative to the enzymes free in solution. Despite representative high-resolution structures of all of the individual modules of the cellulosome, this mechanism of enzymatic synergy remains poorly understood. Consequently, a model of the entire cellulosome and a detailed picture of intermodular contacts will provide more detailed insight into cellulosome activity. Toward this goal, we have solved the structure of a multimodular heterodimeric complex from Clostridium thermocellum composed of the type-II cohesin module of the cell surface protein SdbA bound to a trimodular C-terminal fragment of the scaffoldin subunit CipA to a resolution of 1.95 {angstrom}. The linker that connects the ninth type-I cohesin module and the X module has elevated temperature factors, reflecting an inherent flexibility within this region. Interestingly, a novel dimer interface was observed between CipA and a second, symmetry-related CipA molecule within the crystal structure, mediated by contacts between a type-I cohesin and an X module of a symmetry mate, resulting in two intertwined scaffoldins. Sedimentation velocity experiments confirmed that dimerization also occurs in solution. These observations support the intriguing possibility that individual cellulosomes can associate with one another via inter-scaffoldin interactions, which may play a role in the mechanism of action of the complex.},

  doi          = {},

  url          = {https://www.osti.gov/biblio/1041878},
  journal      = {Journal of Molecular Biology},

  issn         = {0022-2836},

  number       = 4,

  volume       = 396,

  place        = {United States},

  year         = {Sat Dec 31 00:00:00 EST 2011},

  month        = {Sat Dec 31 00:00:00 EST 2011}

}

Copy to clipboard

Journal Article:

Other availability

Find in Google Scholar

Search WorldCat to find libraries that may hold this journal

Save / Share:

Export Metadata

Save to My Library

Similar records in OSTI.GOV collections:

Purification and Crystallization of a Multimodular Heterotrimeric Complex Containing Both Type I and Type II Cohesin-dockerin Interactions from the Cellulosome of Clostridium thermocellum

Journal Article Currie, M; Adams, J; Ali, S; ... - Acta Crystallographica Section F: Structural Biology and Crystallization Communications

The multimodular scaffoldin subunit CipA is the central component of the cellulosome, a multienzyme plant cell-wall-degrading complex, from Clostridium thermocellum. It captures secreted cellulases and hemicellulases and anchors the entire complex to the cell surface via high-affinity calcium-dependent interactions between cohesin and dockerin modules termed type I and type II interactions. The crystallization of a heterotrimeric complex comprising the type II cohesin module from the cell-surface protein SdbA, a trimodular C-terminal fragment of the scaffoldin CipA and the type I dockerin module from the CelD cellulase is reported. The crystals belonged to space group P2{sub 1}2{sub 1}2{sub 1}, with unit-cellmore »« less
Purification and crystallization of a trimodular complex comprising the type II cohesin–dockerin interaction from the cellulosome of Clostridium thermocellum

Journal Article Adams, Jarrett; Pal, Gour; Yam, Katherine; ... - Acta Crystallographica. Section F

A trimodular complex comprising the type II cohesin–dockerin interaction from the cellulosome of C. thermocellum has been purified and crystallized by the hanging-drop vapour-diffusion method. A native crystal and a selenomethionine derivative have been analyzed using X-ray diffraction. The high-affinity calcium-mediated type II cohesin–dockerin interaction is responsible for the attachment of the multi-enzyme cellulose-degrading complex, termed the cellulosome, to the cell surface of the thermophilic anaerobe Clostridium thermocellum. A trimodular 40 kDa complex comprising the SdbA type II cohesin and the the CipA type II dockerin–X module modular pair from the cellulosome of C. thermocellum has been crystallized. The crystalsmore »« less
https://doi.org/10.1107/S1744309104025837
Impact of Pretreated Switchgrass and Biomass Carbohydrates on Clostridium thermocellum 27405 Cellulosome Composition- a Quantitative Proteomic Analysis

Journal Article Raman, Babu; Pan, Chongle; McKeown, Catherine; ... - PLoS ONE

The anaerobic thermophilic bacterium Clostridium thermocellum is a cellulolytic organism capable of hydrolyzing cellulose and fermenting the hydrolysis products to ethanol and other metabolic products. C. thermocellum achieves efficient cellulose hydrolysis using multiprotein extracellular enzymatic complexes, termed the cellulosomes. In this study, we used quantitative proteomics (multidimensional LC-MS/MS and 15N-metabolic labeling) to measure relative changes in levels of cellulosomal subunit proteins (per CipA scaffoldin basis) when C. thermocellum was grown on a variety of carbon sources [dilute-acid pretreated switchgrass, cellobiose, amorphous cellulose, crystalline cellulose (Avicel) and combinations of crystalline cellulose with pectin or xylan or both]. Cellulosome samples isolated frommore »« less
https://doi.org/10.1371/journal.pone.0005271
Mechanism of Bacterial Cell-Surface Attachment Revealed by the Structure of Cellulosomal Type II Cohesin-dockerin Complex

Journal Article Adams, J; Pal, G; Jia, Z; ... - Proceedings of the National Academy of Sciences of the USA

Bacterial cell-surface attachment of macromolecular complexes maintains the microorganism in close proximity to extracellular substrates and allows for optimal uptake of hydrolytic byproducts. The cellulosome is a large multienzyme complex used by many anaerobic bacteria for the efficient degradation of plant cell-wall polysaccharides. The mechanism of cellulosome retention to the bacterial cell surface involves a calcium-mediated protein-protein interaction between the dockerin (Doc) module from the cellulosomal scaffold and a cohesin (Coh) module of cell-surface proteins located within the proteoglycan layer. Here, we report the structure of an ultra-high-affinity (K{sub a} = 1.44 x 10{sup 10} M{sup 1-}) complex between typemore »« less
https://doi.org/10.1073/pnas.0507109103
Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system

Journal Article Zhivin, Olga; Dassa, Bareket; Moraïs, Sarah; ... - Biotechnology for Biofuels

The organization of the B. cellulosolvens cellulosome is unique compared to previously described cellulosome systems. In contrast to all other known cellulosomes, the cohesin types are reversed for all scaffoldins i.e., the type II cohesins are located on the enzyme-integrating primary scaffoldin, whereas the type I cohesins are located on the anchoring scaffoldins. Many of the type II dockerin-bearing ORFs include X60 modules, which are known to stabilize type II cohesin–dockerin interactions. In the present work, we focused on revealing the architectural arrangement of cellulosome structure in this bacterium by examining numerous interactions between the various cohesin and dockerin modules.more »« less
Cited by 21
https://doi.org/10.1186/s13068-017-0898-6

Full Text Available

Similar Records