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Title: 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 » 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.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [4];  [5]; ORCiD logo [1]
  1. Weizmann Inst. of Science, Rehovot (Israel). Dept. of Biomolecular Sciences
  2. 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)
  3. 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
  4. Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France). Architecture et Fonction des Macromolecules Biologiques
  5. Tel Aviv Univ., Ramat Aviv (Israel). Dept. of Molecular Microbiology and Biotechnology
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Israel Science Foundation (ISF); United States-Israel Binational Science Foundation (BSF); National Natural Science Foundation of China (NNSFC)
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. doi: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. doi: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 = {2017},
month = {9}
}

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Cited by: 14 works
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Works referenced in this record:

The Cellulosomes: Multienzyme Machines for Degradation of Plant Cell Wall Polysaccharides
journal, October 2004


Cohesin-Dockerin Interaction in Cellulosome Assembly: A SINGLE HYDROXYL GROUP OF A DOCKERIN DOMAIN DISTINGUISHES BETWEEN NONRECOGNITION AND HIGH AFFINITY RECOGNITION
journal, January 2001

  • Mechaly, Adva; Fierobe, Henri-Pierre; Belaich, Anne
  • Journal of Biological Chemistry, Vol. 276, Issue 13
  • DOI: 10.1074/jbc.M009237200

A cohesin domain from Clostridium thermocellum: the crystal structure provides new insights into cellulosome assembly
journal, March 1997


A synthetic biology approach for evaluating the functional contribution of designer cellulosome components to deconstruction of cellulosic substrates
journal, January 2013


Domain structure of the Acetogenium kivui surface layer revealed by electron crystallography and sequence analysis.
journal, March 1994


Sequencing of a Clostridium thermocellum gene (cipA) encoding the cellulosomal S L -protein reveals an unusual degree of internal homology
journal, April 1993


A Scaffoldin of the Bacteroides cellulosolvens Cellulosome That Contains 11 Type II Cohesins
journal, September 2000


Increased cellulose hydrolysis by Bacteroides cellulosolvens in a simplified synthetic medium
journal, December 1985


The cellulosomes from Clostridium cellulolyticum
journal, June 2009


Standalone cohesin as a molecular shuttle in cellulosome assembly
journal, April 2015


Characterization of All Family-9 Glycoside Hydrolases Synthesized by the Cellulosome-producing Bacterium Clostridium cellulolyticum
journal, January 2014

  • Ravachol, Julie; Borne, Romain; Tardif, Chantal
  • Journal of Biological Chemistry, Vol. 289, Issue 11
  • DOI: 10.1074/jbc.M113.545046

Broad phylogeny and functionality of cellulosomal components in the bovine rumen microbiome
journal, October 2016

  • Bensoussan, Lizi; Moraïs, Sarah; Dassa, Bareket
  • Environmental Microbiology, Vol. 19, Issue 1
  • DOI: 10.1111/1462-2920.13561

Cellulosomics of the cellulolytic thermophile Clostridium clariflavum
journal, January 2014

  • Artzi, Lior; Dassa, Bareket; Borovok, Ilya
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/1754-6834-7-100

The potential of cellulases and cellulosomes for cellulosic waste management
journal, June 2007


Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities
journal, February 2016


Cellulosomal Scaffoldin-Like Proteins from Ruminococcus flavefaciens
journal, March 2001


SignalP 4.0: discriminating signal peptides from transmembrane regions
journal, September 2011

  • Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar
  • Nature Methods, Vol. 8, Issue 10
  • DOI: 10.1038/nmeth.1701

Cellulosome-like entities inBacteroides cellulosolvens
journal, January 1991

  • Lamed, Raphael; Morag (Morgenstern), Ely; Mor-Yosef, Orly
  • Current Microbiology, Vol. 22, Issue 1
  • DOI: 10.1007/BF02106209

Near-Complete Genome Sequence of the Cellulolytic Bacterium Bacteroides ( Pseudobacteroides ) cellulosolvens ATCC 35603
journal, September 2015


Enhancing anaerobic digestion of lignocellulosic materials in excess sludge by bioaugmentation and pre-treatment
journal, March 2016


Clostridium clariflavum: Key Cellulosome Players Are Revealed by Proteomic Analysis
journal, May 2015


Cellulosomes—Structure and Ultrastructure
journal, December 1998

  • Bayer, Edward A.; Shimon, Linda J. W.; Shoham, Yuval
  • Journal of Structural Biology, Vol. 124, Issue 2-3
  • DOI: 10.1006/jsbi.1998.4065

Fuelling the future: microbial engineering for the production of sustainable biofuels
journal, March 2016

  • Liao, James C.; Mi, Luo; Pontrelli, Sammy
  • Nature Reviews Microbiology, Vol. 14, Issue 5
  • DOI: 10.1038/nrmicro.2016.32

Conversion of cellulose to sugars by resting cells of a mesophilic anaerobe,Bacteriodes cellulosolvens
journal, July 1985

  • Giuliano, Christine; Khan, A. W.
  • Biotechnology and Bioengineering, Vol. 27, Issue 7
  • DOI: 10.1002/bit.260270708

Cellulosomes: Highly Efficient Nanomachines Designed to Deconstruct Plant Cell Wall Complex Carbohydrates
journal, June 2010


Combined Crystal Structure of a Type I Cohesin: MUTATION AND AFFINITY BINDING STUDIES REVEAL STRUCTURAL DETERMINANTS OF COHESIN-DOCKERIN SPECIFICITIES
journal, May 2015

  • Cameron, Kate; Weinstein, Jonathan Y.; Zhivin, Olga
  • Journal of Biological Chemistry, Vol. 290, Issue 26
  • DOI: 10.1074/jbc.M115.653303

Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides
journal, December 2016

  • Artzi, Lior; Bayer, Edward A.; Moraïs, Sarah
  • Nature Reviews Microbiology, Vol. 15, Issue 2
  • DOI: 10.1038/nrmicro.2016.164

Bacteroides cellulosolvens sp. nov., a Cellulolytic Species from Sewage Sludge
journal, April 1984

  • Murray, W. D.; Sowden, L. C.; Colvin, J. R.
  • International Journal of Systematic Bacteriology, Vol. 34, Issue 2
  • DOI: 10.1099/00207713-34-2-185

Matching fusion protein systems for affinity analysis of two interacting families of proteins: the cohesin-dockerin interaction
journal, January 2005

  • Barak, Yoav; Handelsman, Tal; Nakar, David
  • Journal of Molecular Recognition, Vol. 18, Issue 6
  • DOI: 10.1002/jmr.749

Diversity and Strain Specificity of Plant Cell Wall Degrading Enzymes Revealed by the Draft Genome of Ruminococcus flavefaciens FD-1
journal, August 2009


Two components of an extracellular protein aggregate of Clostridium thermocellum together degrade crystalline cellulose
journal, March 1988

  • Wu, J. H. David; Orme-Johnson, William H.; Demain, Arnold L.
  • Biochemistry, Vol. 27, Issue 5
  • DOI: 10.1021/bi00405a048

Cellulosome gene cluster analysis for gauging the diversity of the ruminal cellulolytic bacterium Ruminococcus flavefaciens
journal, August 2008


Abundance and Diversity of Dockerin-Containing Proteins in the Fiber-Degrading Rumen Bacterium, Ruminococcus flavefaciens FD-1
journal, August 2010


Acetivibrio cellulolyticus and Bacteroides cellulosolvens are members of the greater clostridial assemblage
journal, December 1994


Crystal Structure of an Uncommon Cellulosome-Related Protein Module from Ruminococcus flavefaciens That Resembles Papain-Like Cysteine Peptidases
journal, February 2013


Role of scaffolding protein CipC of Clostridium cellulolyticum in cellulose degradation.
journal, May 1997


Binding of S-layer homology modules from Clostridium thermocellum SdbA to peptidoglycans
journal, July 2005

  • Zhao, Guangshan; Ali, Ehsan; Sakka, Makiko
  • Applied Microbiology and Biotechnology, Vol. 70, Issue 4
  • DOI: 10.1007/s00253-005-0079-6

Cohesin-dockerin microarray: Diverse specificities between two complementary families of interacting protein modules
journal, March 2008


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

Evidence for a dual binding mode of dockerin modules to cohesins
journal, February 2007

  • Carvalho, A. L.; Dias, F. M. V.; Nagy, T.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 9
  • DOI: 10.1073/pnas.0611173104

Ruminococcal cellulosome systems from rumen to human: Human ruminococcal cellulosome
journal, May 2015

  • Ben David, Yonit; Dassa, Bareket; Borovok, Ilya
  • Environmental Microbiology, Vol. 17, Issue 9
  • DOI: 10.1111/1462-2920.12868

Cohesin-dockerin recognition in cellulosome assembly: Experiment versus hypothesis
journal, May 2000


The cellulosome — A treasure-trove for biotechnology
journal, September 1994


Genome-wide analysis of Acetivibrio cellulolyticus provides a blueprint of an elaborate cellulosome system
journal, January 2012


The Clostridium cellulolyticum Dockerin Displays a Dual Binding Mode for Its Cohesin Partner
journal, April 2008

  • Pinheiro, Benedita A.; Proctor, Mark R.; Martinez-Fleites, Carlos
  • Journal of Biological Chemistry, Vol. 283, Issue 26
  • DOI: 10.1074/jbc.M801533200

Expression, purification and structural characterization of the scaffoldin hydrophilic X-module from the cellulosome of Clostridium thermocellum
journal, December 2004

  • Adams, Jarrett J.; Jang, Christopher J.; Spencer, Holly L.
  • Protein Expression and Purification, Vol. 38, Issue 2
  • DOI: 10.1016/j.pep.2004.08.018

Conservation and Divergence in Cellulosome Architecture between Two Strains of Ruminococcus flavefaciens
journal, September 2006

  • Jindou, S.; Borovok, I.; Rincon, M. T.
  • Journal of Bacteriology, Vol. 188, Issue 22
  • DOI: 10.1128/JB.00973-06

Functional insights into the role of novel type I cohesin and dockerin domains from Clostridium thermocellum
journal, December 2009

  • Pinheiro, Benedita A.; Gilbert, Harry J.; Sakka, Kazutaka
  • Biochemical Journal, Vol. 424, Issue 3
  • DOI: 10.1042/BJ20091152

Rumen Cellulosomics: Divergent Fiber-Degrading Strategies Revealed by Comparative Genome-Wide Analysis of Six Ruminococcal Strains
journal, July 2014


Intramolecular clasp of the cellulosomal Ruminococcus flavefaciens ScaA dockerin module confers structural stability
journal, January 2013


Draft Genome Sequences for Clostridium thermocellum Wild-Type Strain YS and Derived Cellulose Adhesion-Defective Mutant Strain AD2
journal, May 2012

  • Brown, S. D.; Lamed, R.; Morag, E.
  • Journal of Bacteriology, Vol. 194, Issue 12
  • DOI: 10.1128/JB.00473-12

    Works referencing / citing this record:

    Creation of a functional hyperthermostable designer cellulosome
    journal, February 2019

    • Kahn, Amaranta; Moraïs, Sarah; Galanopoulou, Anastasia P.
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1386-y

    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
    • DOI: 10.1186/s13068-019-1447-2

    Secretomic analyses of Ruminiclostridium papyrosolvens reveal its enzymatic basis for lignocellulose degradation
    journal, July 2019


    Structural basis of oligosaccharide processing by glycosaminoglycan sulfotransferases
    journal, June 2018

    • Gesteira, Tarsis F.; Coulson-Thomas, Vivien J.
    • Glycobiology, Vol. 28, Issue 11
    • DOI: 10.1093/glycob/cwy055

    Structural basis of oligosaccharide processing by glycosaminoglycan sulfotransferases
    journal, June 2018

    • Gesteira, Tarsis F.; Coulson-Thomas, Vivien J.
    • Glycobiology, Vol. 28, Issue 11
    • DOI: 10.1093/glycob/cwy055

    Creation of a functional hyperthermostable designer cellulosome
    journal, February 2019

    • Kahn, Amaranta; Moraïs, Sarah; Galanopoulou, Anastasia P.
    • Biotechnology for Biofuels, Vol. 12, Issue 1
    • DOI: 10.1186/s13068-019-1386-y

    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
    • DOI: 10.1186/s13068-019-1447-2

    Secretomic analyses of Ruminiclostridium papyrosolvens reveal its enzymatic basis for lignocellulose degradation
    journal, July 2019


    Inducing effects of cellulosic hydrolysate components of lignocellulose on cellulosome synthesis in Clostridium thermocellum
    journal, June 2018