Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system
Abstract
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. In total, we cloned and expressed 43 representative cohesins and 27 dockerins. The results revealed various possible architectures of cell-anchored and cell-free cellulosomes, which serve to assemble distinctive cellulosome types via three distinct cohesin–dockerin specificities: type I, type II, and a novel-type designated R (distinct from type III interactions, predominant in ruminococcal cellulosomes). The results of this study provide novel insight into the architecture and function of the most intricate and extensive cellulosomal system known today, thereby extending significantly our overall knowledge base of cellulosome systems and their components. The robust cellulosome system of B. cellulosolvens, with its unique bindingmore »
- Authors:
-
[1]
- Weizmann Inst. of Science, Rehovot (Israel). Dept. of Biomolecular Sciences
- Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
- Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division, Energy and Environment Directorate
- Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France). Architecture et Fonction des Macromolecules Biologiques
- Tel Aviv Univ., Ramat Aviv (Israel). Dept. of Molecular Microbiology and Biotechnology
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Israel Science Foundation (ISF); United States-Israel Binational Science Foundation (BSF); National Natural Science Foundation of China (NSFC)
- OSTI Identifier:
- 1394357
- Grant/Contract Number:
- AC05-00OR22725; 2566/16; 1349
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Biotechnology for Biofuels
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1754-6834
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 09 BIOMASS FUELS; cohesion; dockerin; scaffoldin; cellulolytic bacteria; CBM; cellulases; Glgycoside hydrolases
Citation Formats
Zhivin, Olga, Dassa, Bareket, Moraïs, Sarah, Utturkar, Sagar M., Brown, Steven D., Henrissat, Bernard, Lamed, Raphael, and Bayer, Edward A. Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system. United States: N. p., 2017.
Web. doi:10.1186/s13068-017-0898-6.
Zhivin, Olga, Dassa, Bareket, Moraïs, Sarah, Utturkar, Sagar M., Brown, Steven D., Henrissat, Bernard, Lamed, Raphael, & Bayer, Edward A. Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system. United States. https://doi.org/10.1186/s13068-017-0898-6
Zhivin, Olga, Dassa, Bareket, Moraïs, Sarah, Utturkar, Sagar M., Brown, Steven D., Henrissat, Bernard, Lamed, Raphael, and Bayer, Edward A. Thu .
"Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system". United States. https://doi.org/10.1186/s13068-017-0898-6. https://www.osti.gov/servlets/purl/1394357.
@article{osti_1394357,
title = {Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system},
author = {Zhivin, Olga and Dassa, Bareket and Moraïs, Sarah and Utturkar, Sagar M. and Brown, Steven D. and Henrissat, Bernard and Lamed, Raphael and Bayer, Edward A.},
abstractNote = {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. In total, we cloned and expressed 43 representative cohesins and 27 dockerins. The results revealed various possible architectures of cell-anchored and cell-free cellulosomes, which serve to assemble distinctive cellulosome types via three distinct cohesin–dockerin specificities: type I, type II, and a novel-type designated R (distinct from type III interactions, predominant in ruminococcal cellulosomes). The results of this study provide novel insight into the architecture and function of the most intricate and extensive cellulosomal system known today, thereby extending significantly our overall knowledge base of cellulosome systems and their components. The robust cellulosome system of B. cellulosolvens, with its unique binding specificities and reversal of cohesin–dockerin types, has served to amend our view of the cellulosome paradigm. Revealing new cellulosomal interactions and arrangements is critical for designing high-efficiency artificial cellulosomes for conversion of plant-derived cellulosic biomass towards improved production of biofuels.},
doi = {10.1186/s13068-017-0898-6},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 10,
place = {United States},
year = {Thu Sep 07 00:00:00 EDT 2017},
month = {Thu Sep 07 00:00:00 EDT 2017}
}
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A Scaffoldin of the Bacteroides cellulosolvens Cellulosome That Contains 11 Type II Cohesins
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Genome-wide analysis of Acetivibrio cellulolyticus provides a blueprint of an elaborate cellulosome system
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A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates
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Cellulosomics of the cellulolytic thermophile Clostridium clariflavum
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Rumen Cellulosomics: Divergent Fiber-Degrading Strategies Revealed by Comparative Genome-Wide Analysis of Six Ruminococcal Strains
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Works referencing / citing this record:
Dual binding in cohesin-dockerin complexes: the energy landscape and the role of short, terminal segments of the dockerin module
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- Wojciechowski, Michał; Różycki, Bartosz; Huy, Pham Dinh Quoc
- Scientific Reports, Vol. 8, Issue 1
Regulation of biomass degradation by alternative σ factors in cellulolytic clostridia
journal, July 2018
- Ortiz de Ora, Lizett; Lamed, Raphael; Liu, Ya-Jun
- Scientific Reports, Vol. 8, Issue 1
Changing surface grafting density has an effect on the activity of immobilized xylanase towards natural polysaccharides
journal, April 2019
- Montanier, Cédric Y.; Fanuel, Mathieu; Rogniaux, Hélène
- Scientific Reports, Vol. 9, Issue 1
Structural basis of oligosaccharide processing by glycosaminoglycan sulfotransferases
journal, June 2018
- Gesteira, Tarsis F.; Coulson-Thomas, Vivien J.
- Glycobiology, Vol. 28, Issue 11
Inducing effects of cellulosic hydrolysate components of lignocellulose on cellulosome synthesis in Clostridium thermocellum
journal, June 2018
- Li, Renmin; Feng, Yingang; Liu, Shiyue
- Microbial Biotechnology, Vol. 11, Issue 5
Creation of a functional hyperthermostable designer cellulosome
journal, February 2019
- Kahn, Amaranta; Moraïs, Sarah; Galanopoulou, Anastasia P.
- Biotechnology for Biofuels, Vol. 12, Issue 1
Unraveling essential cellulosomal components of the (Pseudo)Bacteroides cellulosolvens reveals an extensive reservoir of novel catalytic enzymes
journal, May 2019
- Zhivin-Nissan, Olga; Dassa, Bareket; Morag, Ely
- Biotechnology for Biofuels, Vol. 12, Issue 1
Secretomic analyses of Ruminiclostridium papyrosolvens reveal its enzymatic basis for lignocellulose degradation
journal, July 2019
- Ren, Zhenxing; You, Wuxin; Wu, Shasha
- Biotechnology for Biofuels, Vol. 12, Issue 1
Pan-Cellulosomics of Mesophilic Clostridia: Variations on a Theme
journal, November 2017
- Dassa, Bareket; Borovok, Ilya; Lombard, Vincent
- Microorganisms, Vol. 5, Issue 4
Dual binding in cohesin-dockerin complexes: the energy landscape and the role of short, terminal segments of the dockerin module
journal, March 2018
- Wojciechowski, Michał; Różycki, Bartosz; Huy, Pham Dinh Quoc
- Scientific Reports, Vol. 8, Issue 1
Regulation of biomass degradation by alternative σ factors in cellulolytic clostridia
journal, July 2018
- Ortiz de Ora, Lizett; Lamed, Raphael; Liu, Ya-Jun
- Scientific Reports, Vol. 8, Issue 1
Changing surface grafting density has an effect on the activity of immobilized xylanase towards natural polysaccharides
journal, April 2019
- Montanier, Cédric Y.; Fanuel, Mathieu; Rogniaux, Hélène
- Scientific Reports, Vol. 9, Issue 1
Creation of a functional hyperthermostable designer cellulosome
journal, February 2019
- Kahn, Amaranta; Moraïs, Sarah; Galanopoulou, Anastasia P.
- Biotechnology for Biofuels, Vol. 12, Issue 1
Secretomic analyses of Ruminiclostridium papyrosolvens reveal its enzymatic basis for lignocellulose degradation
journal, July 2019
- Ren, Zhenxing; You, Wuxin; Wu, Shasha
- Biotechnology for Biofuels, Vol. 12, Issue 1
Pan-Cellulosomics of Mesophilic Clostridia: Variations on a Theme
journal, November 2017
- Dassa, Bareket; Borovok, Ilya; Lombard, Vincent
- Microorganisms, Vol. 5, Issue 4
The Cellulosome Paradigm in An Extreme Alkaline Environment
journal, September 2019
- Phitsuwan,
- Microorganisms, Vol. 7, Issue 9