Higher order scaffoldin assembly in Ruminococcus flavefaciens cellulosome is coordinated by a discrete cohesin-dockerin interaction

Pedro Bule, Virgínia M. R. Pires, Victor D. Alves, Ana Luísa Carvalho, José A. M. Prates, Luís M. A. Ferreira, Steven P. Smith, Harry J. Gilbert, Ilit Noach, Edward A. Bayer, Shabir Najmudin, Carlos M.G.A. Fontes

Research output: Contribution to journalArticle

1 Citation (Scopus)
8 Downloads (Pure)

Abstract

Cellulosomes are highly sophisticated molecular nanomachines that participate in the deconstruction of complex polysaccharides, notably cellulose and hemicellulose. Cellulosomal assembly is orchestrated by the interaction of enzyme-borne dockerin (Doc) modules to tandem cohesin (Coh) modules of a non-catalytic primary scaffoldin. In some cases, as exemplified by the cellulosome of the major cellulolytic ruminal bacterium Ruminococcus flavefaciens, primary scaffoldins bind to adaptor scaffoldins that further interact with the cell surface via anchoring scaffoldins, thereby increasing cellulosome complexity. Here we elucidate the structure of the unique Doc of R. flavefaciens FD-1 primary scaffoldin ScaA, bound to Coh 5 of the adaptor scaffoldin ScaB. The RfCohScaB5-DocScaA complex has an elliptical architecture similar to previously described complexes from a variety of ecological niches. ScaA Doc presents a single-binding mode, analogous to that described for the other two Coh-Doc specificities required for cellulosome assembly in R. flavefaciens. The exclusive reliance on a single-mode of Coh recognition contrasts with the majority of cellulosomes from other bacterial species described to date, where Docs contain two similar Coh-binding interfaces promoting a dual-binding mode. The discrete Coh-Doc interactions observed in ruminal cellulosomes suggest an adaptation to the exquisite properties of the rumen environment.

Original languageEnglish
Article number6987
JournalScientific Reports
Volume8
Issue number1
DOIs
Publication statusPublished - 1 Dec 2018

Fingerprint

Cellulosomes
Ruminococcus
Rumen
Cellulose
Polysaccharides
cohesins
Bacteria
Enzymes

Keywords

  • Clostridium thermocellum
  • Cellulosomes
  • Consolidated bioprocessing

Cite this

Bule, Pedro ; Pires, Virgínia M. R. ; Alves, Victor D. ; Carvalho, Ana Luísa ; Prates, José A. M. ; Ferreira, Luís M. A. ; Smith, Steven P. ; Gilbert, Harry J. ; Noach, Ilit ; Bayer, Edward A. ; Najmudin, Shabir ; Fontes, Carlos M.G.A. / Higher order scaffoldin assembly in Ruminococcus flavefaciens cellulosome is coordinated by a discrete cohesin-dockerin interaction. In: Scientific Reports. 2018 ; Vol. 8, No. 1.
@article{163145738229457b90030a163147a9b9,
title = "Higher order scaffoldin assembly in Ruminococcus flavefaciens cellulosome is coordinated by a discrete cohesin-dockerin interaction",
abstract = "Cellulosomes are highly sophisticated molecular nanomachines that participate in the deconstruction of complex polysaccharides, notably cellulose and hemicellulose. Cellulosomal assembly is orchestrated by the interaction of enzyme-borne dockerin (Doc) modules to tandem cohesin (Coh) modules of a non-catalytic primary scaffoldin. In some cases, as exemplified by the cellulosome of the major cellulolytic ruminal bacterium Ruminococcus flavefaciens, primary scaffoldins bind to adaptor scaffoldins that further interact with the cell surface via anchoring scaffoldins, thereby increasing cellulosome complexity. Here we elucidate the structure of the unique Doc of R. flavefaciens FD-1 primary scaffoldin ScaA, bound to Coh 5 of the adaptor scaffoldin ScaB. The RfCohScaB5-DocScaA complex has an elliptical architecture similar to previously described complexes from a variety of ecological niches. ScaA Doc presents a single-binding mode, analogous to that described for the other two Coh-Doc specificities required for cellulosome assembly in R. flavefaciens. The exclusive reliance on a single-mode of Coh recognition contrasts with the majority of cellulosomes from other bacterial species described to date, where Docs contain two similar Coh-binding interfaces promoting a dual-binding mode. The discrete Coh-Doc interactions observed in ruminal cellulosomes suggest an adaptation to the exquisite properties of the rumen environment.",
keywords = "Clostridium thermocellum, Cellulosomes, Consolidated bioprocessing",
author = "Pedro Bule and Pires, {Virg{\'i}nia M. R.} and Alves, {Victor D.} and Carvalho, {Ana Lu{\'i}sa} and Prates, {Jos{\'e} A. M.} and Ferreira, {Lu{\'i}s M. A.} and Smith, {Steven P.} and Gilbert, {Harry J.} and Ilit Noach and Bayer, {Edward A.} and Shabir Najmudin and Fontes, {Carlos M.G.A.}",
note = "The authors acknowledge financial support from Fundacao para a Ciencia e a Tecnologia (Lisbon, Portugal) through grants PTDC/BIA-MIC/5947/2014, RECI/BBB-BEP/0124/2012 while PB and VMRP were supported by the individual fellowships SFRH/BD/86821/2012 and IF/01621/2013, respectively. The authors also acknowledge Professor Maria Joao Romao for access to the crystallization facilities of the Protein Crystallography Group in the Faculty of Science and Technology, Universidade NOVA de Lisboa, as well as the Soleil synchrotron, L'Orme des Merisiers, Saint-Aubin, France, (beamline PROXIMA-1) for access and technical support during data collection, and the European Community's Seventh Framework Programme (FP7/2007-2013) under BioStruct-X (grant agreement No. 283570, proposal number: Biostruct-X_4399) for funding. The Unidade de Ciencias Biomoleculares Aplicadas (UCIBIO- REQUIMTE) is financed by national funds from Fundacao para a Ciencia e Tecnologia/Ministerio da Educacao e Ciencia (FCT/ME) (UID/Multi/04378/2013) and co-financed by the European Regional Development Fund under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728).",
year = "2018",
month = "12",
day = "1",
doi = "10.1038/s41598-018-25171-8",
language = "English",
volume = "8",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",
number = "1",

}

Bule, P, Pires, VMR, Alves, VD, Carvalho, AL, Prates, JAM, Ferreira, LMA, Smith, SP, Gilbert, HJ, Noach, I, Bayer, EA, Najmudin, S & Fontes, CMGA 2018, 'Higher order scaffoldin assembly in Ruminococcus flavefaciens cellulosome is coordinated by a discrete cohesin-dockerin interaction', Scientific Reports, vol. 8, no. 1, 6987. https://doi.org/10.1038/s41598-018-25171-8

Higher order scaffoldin assembly in Ruminococcus flavefaciens cellulosome is coordinated by a discrete cohesin-dockerin interaction. / Bule, Pedro; Pires, Virgínia M. R.; Alves, Victor D.; Carvalho, Ana Luísa; Prates, José A. M.; Ferreira, Luís M. A.; Smith, Steven P.; Gilbert, Harry J.; Noach, Ilit; Bayer, Edward A.; Najmudin, Shabir; Fontes, Carlos M.G.A.

In: Scientific Reports, Vol. 8, No. 1, 6987, 01.12.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Higher order scaffoldin assembly in Ruminococcus flavefaciens cellulosome is coordinated by a discrete cohesin-dockerin interaction

AU - Bule, Pedro

AU - Pires, Virgínia M. R.

AU - Alves, Victor D.

AU - Carvalho, Ana Luísa

AU - Prates, José A. M.

AU - Ferreira, Luís M. A.

AU - Smith, Steven P.

AU - Gilbert, Harry J.

AU - Noach, Ilit

AU - Bayer, Edward A.

AU - Najmudin, Shabir

AU - Fontes, Carlos M.G.A.

N1 - The authors acknowledge financial support from Fundacao para a Ciencia e a Tecnologia (Lisbon, Portugal) through grants PTDC/BIA-MIC/5947/2014, RECI/BBB-BEP/0124/2012 while PB and VMRP were supported by the individual fellowships SFRH/BD/86821/2012 and IF/01621/2013, respectively. The authors also acknowledge Professor Maria Joao Romao for access to the crystallization facilities of the Protein Crystallography Group in the Faculty of Science and Technology, Universidade NOVA de Lisboa, as well as the Soleil synchrotron, L'Orme des Merisiers, Saint-Aubin, France, (beamline PROXIMA-1) for access and technical support during data collection, and the European Community's Seventh Framework Programme (FP7/2007-2013) under BioStruct-X (grant agreement No. 283570, proposal number: Biostruct-X_4399) for funding. The Unidade de Ciencias Biomoleculares Aplicadas (UCIBIO- REQUIMTE) is financed by national funds from Fundacao para a Ciencia e Tecnologia/Ministerio da Educacao e Ciencia (FCT/ME) (UID/Multi/04378/2013) and co-financed by the European Regional Development Fund under the PT2020 Partnership Agreement (POCI-01-0145-FEDER-007728).

PY - 2018/12/1

Y1 - 2018/12/1

N2 - Cellulosomes are highly sophisticated molecular nanomachines that participate in the deconstruction of complex polysaccharides, notably cellulose and hemicellulose. Cellulosomal assembly is orchestrated by the interaction of enzyme-borne dockerin (Doc) modules to tandem cohesin (Coh) modules of a non-catalytic primary scaffoldin. In some cases, as exemplified by the cellulosome of the major cellulolytic ruminal bacterium Ruminococcus flavefaciens, primary scaffoldins bind to adaptor scaffoldins that further interact with the cell surface via anchoring scaffoldins, thereby increasing cellulosome complexity. Here we elucidate the structure of the unique Doc of R. flavefaciens FD-1 primary scaffoldin ScaA, bound to Coh 5 of the adaptor scaffoldin ScaB. The RfCohScaB5-DocScaA complex has an elliptical architecture similar to previously described complexes from a variety of ecological niches. ScaA Doc presents a single-binding mode, analogous to that described for the other two Coh-Doc specificities required for cellulosome assembly in R. flavefaciens. The exclusive reliance on a single-mode of Coh recognition contrasts with the majority of cellulosomes from other bacterial species described to date, where Docs contain two similar Coh-binding interfaces promoting a dual-binding mode. The discrete Coh-Doc interactions observed in ruminal cellulosomes suggest an adaptation to the exquisite properties of the rumen environment.

AB - Cellulosomes are highly sophisticated molecular nanomachines that participate in the deconstruction of complex polysaccharides, notably cellulose and hemicellulose. Cellulosomal assembly is orchestrated by the interaction of enzyme-borne dockerin (Doc) modules to tandem cohesin (Coh) modules of a non-catalytic primary scaffoldin. In some cases, as exemplified by the cellulosome of the major cellulolytic ruminal bacterium Ruminococcus flavefaciens, primary scaffoldins bind to adaptor scaffoldins that further interact with the cell surface via anchoring scaffoldins, thereby increasing cellulosome complexity. Here we elucidate the structure of the unique Doc of R. flavefaciens FD-1 primary scaffoldin ScaA, bound to Coh 5 of the adaptor scaffoldin ScaB. The RfCohScaB5-DocScaA complex has an elliptical architecture similar to previously described complexes from a variety of ecological niches. ScaA Doc presents a single-binding mode, analogous to that described for the other two Coh-Doc specificities required for cellulosome assembly in R. flavefaciens. The exclusive reliance on a single-mode of Coh recognition contrasts with the majority of cellulosomes from other bacterial species described to date, where Docs contain two similar Coh-binding interfaces promoting a dual-binding mode. The discrete Coh-Doc interactions observed in ruminal cellulosomes suggest an adaptation to the exquisite properties of the rumen environment.

KW - Clostridium thermocellum

KW - Cellulosomes

KW - Consolidated bioprocessing

UR - http://www.scopus.com/inward/record.url?scp=85046619629&partnerID=8YFLogxK

U2 - 10.1038/s41598-018-25171-8

DO - 10.1038/s41598-018-25171-8

M3 - Article

VL - 8

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 6987

ER -