TY - JOUR
T1 - A dual cohesin–dockerin complex binding mode in Bacteroides cellulosolvens contributes to the size and complexity of its cellulosome
AU - Duarte, Marlene
AU - Viegas, Aldino
AU - Prates, José A.M.
AU - Ferreira, Luís M.A.
AU - Najmudin, Shabir
AU - Cabrita, Eurico J.
AU - Carvalho, Ana Luísa
AU - Fontes, Carlos M.G.A.
AU - Bule, Pedro
N1 - Funding Information:
Funding and additional information—This work was supported by the Portuguese Foundation for Science and Technology (FCT-MCTES) through the Centro de Investigação Interdisciplinar em Sanidade Animal (CIISA) grant UIDB/00276/2020, the Applied Molecular Biosciences Unit (UCIBIO) grant UIDB/04378/2020, and through the National Project grant RECI/BBB-BEP/0124/2012. M. D. is supported by a PhD studentship (SFRH/BD/146965/2019) from FCT-MCTES. A. V. was supported by a PhD studentship (SFRH/BD/35992/2007) FCT-MCTES.
Publisher Copyright:
© 2021 THE AUTHORS.
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/3/18
Y1 - 2021/3/18
N2 - The Cellulosome is an intricate macromolecular protein complex that centralizes the cellulolytic efforts of many anaerobic microorganisms through the promotion of enzyme synergy and protein stability. The assembly of numerous carbohydrate processing enzymes into a macromolecular multiprotein structure results from the interaction of enzyme-borne dockerin modules with repeated cohesin modules present in noncatalytic scaffold proteins, termed scaffoldins. Cohesin- dockerin (Coh-Doc) modules are typically classified into different types, depending on structural conformation and cellulosome role. Thus, type I Coh-Doc complexes are usually responsible for enzyme integration into the cellulosome, while type II Coh-Doc complexes tether the cellulosome to the bacterial wall. In contrast to other known cellulosomes, cohesin types from Bacteroides cellulosolvens, a cellulosome-producing bacterium capable of utilizing cellulose and cellobiose as carbon sources, 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. It has been previously shown that type I B. cellulosolvens interactions possess a dual-binding mode that adds flexibility to scaffoldin assembly. Herein, we report the structural mechanism of enzyme recruitment into B. cellulosolvens cellulosome and the identification of the molecular determinants of its type II cohesin-dockerin interactions. The results indicate that, unlike other type II complexes, these possess a dual-binding mode of interaction, akin to type I complexes. Therefore, the plasticity of dualbinding mode interactions seems to play a pivotal role in the assembly of B. cellulosolvens cellulosome, which is consistent with its unmatched complexity and size.
AB - The Cellulosome is an intricate macromolecular protein complex that centralizes the cellulolytic efforts of many anaerobic microorganisms through the promotion of enzyme synergy and protein stability. The assembly of numerous carbohydrate processing enzymes into a macromolecular multiprotein structure results from the interaction of enzyme-borne dockerin modules with repeated cohesin modules present in noncatalytic scaffold proteins, termed scaffoldins. Cohesin- dockerin (Coh-Doc) modules are typically classified into different types, depending on structural conformation and cellulosome role. Thus, type I Coh-Doc complexes are usually responsible for enzyme integration into the cellulosome, while type II Coh-Doc complexes tether the cellulosome to the bacterial wall. In contrast to other known cellulosomes, cohesin types from Bacteroides cellulosolvens, a cellulosome-producing bacterium capable of utilizing cellulose and cellobiose as carbon sources, 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. It has been previously shown that type I B. cellulosolvens interactions possess a dual-binding mode that adds flexibility to scaffoldin assembly. Herein, we report the structural mechanism of enzyme recruitment into B. cellulosolvens cellulosome and the identification of the molecular determinants of its type II cohesin-dockerin interactions. The results indicate that, unlike other type II complexes, these possess a dual-binding mode of interaction, akin to type I complexes. Therefore, the plasticity of dualbinding mode interactions seems to play a pivotal role in the assembly of B. cellulosolvens cellulosome, which is consistent with its unmatched complexity and size.
KW - cellulosome cohesin dockerin dual-binding protein complex crystal structure cellulose cellulase
UR - http://www.scopus.com/inward/record.url?scp=85104583307&partnerID=8YFLogxK
U2 - 10.1016/j.jbc.2021.100552
DO - 10.1016/j.jbc.2021.100552
M3 - Article
SN - 0021-9258
VL - 296
SP - 100552
EP - 100564
JO - Journal of Biological Chemistry
JF - Journal of Biological Chemistry
M1 - A84
ER -