Ruminococcal cellulosome systems from rumen to human

Yonit Ben David, Bareket Dassa, Ilya Borovok, Raphael Lamed, Nicole M Koropatkin, Eric C Martens, Bryan A White, Annick Bernalier-Donadille, Sylvia H Duncan, Harry J Flint, Edward A Bayer, Sarah Moraïs

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Abstract

A cellulolytic fiber-degrading bacterium, Ruminococcus champanellensis, was isolated from human faecal samples, and its genome was recently sequenced. Bioinformatic analysis of the R. champanellensis genome revealed numerous cohesin and dockerin modules, the basic elements of the cellulosome, and manual sequencing of partially sequenced genomic segments revealed two large tandem scaffoldin-coding genes that form part of a gene cluster. Representative R. champanellensis dockerins were tested against putative cohesins, and the results revealed three different cohesin-dockerin binding profiles which implied two major types of cellulosome architectures: (i) an intricate cell-bound system and (ii) a simplistic cell-free system composed of a single cohesin-containing scaffoldin. The cell-bound system can adopt various enzymatic architectures, ranging from a single enzyme to a large enzymatic complex comprising up to 11 enzymes. The variety of cellulosomal components together with adaptor proteins may infer a very tight regulation of its components. The cellulosome system of the human gut bacterium R. champanellensis closely resembles that of the bovine rumen bacterium Ruminococcus flavefaciens. The two species contain orthologous gene clusters comprising fundamental components of cellulosome architecture. Since R. champanellensis is the only human colonic bacterium known to degrade crystalline cellulose, it may thus represent a keystone species in the human gut.

Original languageEnglish
Pages (from-to)3407-3426
Number of pages20
JournalEnvironmental Microbiology
Volume17
Issue number9
Early online date3 Apr 2015
DOIs
Publication statusPublished - Sep 2015

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cellulosome
Cellulosomes
Rumen
rumen
Ruminococcus
Bacteria
bacterium
Multigene Family
multigene family
gene
bacteria
genome
digestive system
Ruminococcus flavefaciens
Genome
enzyme
cell free system
keystone species
rumen bacteria
bioinformatics

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David, Y. B., Dassa, B., Borovok, I., Lamed, R., Koropatkin, N. M., Martens, E. C., ... Moraïs, S. (2015). Ruminococcal cellulosome systems from rumen to human. Environmental Microbiology, 17(9), 3407-3426. https://doi.org/10.1111/1462-2920.12868

Ruminococcal cellulosome systems from rumen to human. / David, Yonit Ben; Dassa, Bareket; Borovok, Ilya; Lamed, Raphael; Koropatkin, Nicole M; Martens, Eric C; White, Bryan A; Bernalier-Donadille, Annick; Duncan, Sylvia H; Flint, Harry J; Bayer, Edward A; Moraïs, Sarah.

In: Environmental Microbiology, Vol. 17, No. 9, 09.2015, p. 3407-3426.

Research output: Contribution to journalArticle

David, YB, Dassa, B, Borovok, I, Lamed, R, Koropatkin, NM, Martens, EC, White, BA, Bernalier-Donadille, A, Duncan, SH, Flint, HJ, Bayer, EA & Moraïs, S 2015, 'Ruminococcal cellulosome systems from rumen to human', Environmental Microbiology, vol. 17, no. 9, pp. 3407-3426. https://doi.org/10.1111/1462-2920.12868
David YB, Dassa B, Borovok I, Lamed R, Koropatkin NM, Martens EC et al. Ruminococcal cellulosome systems from rumen to human. Environmental Microbiology. 2015 Sep;17(9):3407-3426. https://doi.org/10.1111/1462-2920.12868
David, Yonit Ben ; Dassa, Bareket ; Borovok, Ilya ; Lamed, Raphael ; Koropatkin, Nicole M ; Martens, Eric C ; White, Bryan A ; Bernalier-Donadille, Annick ; Duncan, Sylvia H ; Flint, Harry J ; Bayer, Edward A ; Moraïs, Sarah. / Ruminococcal cellulosome systems from rumen to human. In: Environmental Microbiology. 2015 ; Vol. 17, No. 9. pp. 3407-3426.
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abstract = "A cellulolytic fiber-degrading bacterium, Ruminococcus champanellensis, was isolated from human faecal samples, and its genome was recently sequenced. Bioinformatic analysis of the R. champanellensis genome revealed numerous cohesin and dockerin modules, the basic elements of the cellulosome, and manual sequencing of partially sequenced genomic segments revealed two large tandem scaffoldin-coding genes that form part of a gene cluster. Representative R. champanellensis dockerins were tested against putative cohesins, and the results revealed three different cohesin-dockerin binding profiles which implied two major types of cellulosome architectures: (i) an intricate cell-bound system and (ii) a simplistic cell-free system composed of a single cohesin-containing scaffoldin. The cell-bound system can adopt various enzymatic architectures, ranging from a single enzyme to a large enzymatic complex comprising up to 11 enzymes. The variety of cellulosomal components together with adaptor proteins may infer a very tight regulation of its components. The cellulosome system of the human gut bacterium R. champanellensis closely resembles that of the bovine rumen bacterium Ruminococcus flavefaciens. The two species contain orthologous gene clusters comprising fundamental components of cellulosome architecture. Since R. champanellensis is the only human colonic bacterium known to degrade crystalline cellulose, it may thus represent a keystone species in the human gut.",
author = "David, {Yonit Ben} and Bareket Dassa and Ilya Borovok and Raphael Lamed and Koropatkin, {Nicole M} and Martens, {Eric C} and White, {Bryan A} and Annick Bernalier-Donadille and Duncan, {Sylvia H} and Flint, {Harry J} and Bayer, {Edward A} and Sarah Mora{\"i}s",
note = "This article is protected by copyright. All rights reserved. The authors appreciate the kind assistance of Miriam Lerner (ImmunArray Ltd. Company, Rehovot, Israel) with experiments involving the MicroGrid II arrayer. This research was supported by a grant (No. 1349) to EAB also from the Israel Science Foundation (ISF) and a grant (No. 24/11) issued to RL by The Sidney E. Frank Foundation also through the ISF. Additional support was obtained from the establishment of an Israeli Center of Research Excellence (I-CORE Center No. 152/11) managed by the Israel Science Foundation, from the United States-Israel Binational Science Foundation (BSF), Jerusalem, Israel, by the Weizmann Institute of Science Alternative Energy Research Initiative (AERI) and the Helmsley Foundation. The authors also appreciate the support of the European Union, Area NMP.2013.1.1-2: Self-assembly of naturally occurring nanosystems: CellulosomePlus Project number: 604530 and an ERA-IB Consortium (EIB.12.022), acronym FiberFuel. HF and SHD acknowledge support from the Scottish Government Food Land and People programme and from BBSRC grant no. BB/L009951/1. In addition, EAB is grateful for a grant from the F. Warren Hellman Grant for Alternative Energy Research in Israel in support of alternative energy research in Israel administered by the Israel Strategic Alternative Energy Foundation (I-SAEF). E.A.B. is the incumbent of The Maynard I. and Elaine Wishner Chair of Bio-organic Chemistry",
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