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Title: Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725

Abstract

Caldicellulosiruptor bescii DSM 6725 utilizes various polysaccharides and grows efficiently on untreated high-lignin grasses and hardwood at an optimum temperature of 80C. It is a promising anaerobic bacterium for studying high-temperature biomass conversion. Its genome contains 2666 proteincoding sequences organized into 1209 operons. Expression of 2196 genes (83%) was confirmed experimentally. At least 322 genes appear to have been obtained by lateral gene transfer (LGT). Putative functions were assigned to 364 conserved/hypothetical protein (C/HP) genes. The genome contains 171 and 88 genes related to carbohydrate transport and utilization, respectively. Growth on cellulose led to the up-regulation of 32 carbohydrate-active (CAZy), 61 sugar transport, 25 transcription factor and 234 C/HP genes. Some C/HPs were overproduced on cellulose or xylan, suggesting their involvement in polysaccharide conversion. A unique feature of the genome is enrichment with genes encoding multi-modular, multi-functional CAZy proteins organized into one large cluster, the products of which are proposed to act synergistically on different components of plant cell walls and to aid the ability of C. bescii to convert plant biomass. The high duplication of CAZy domains coupled with the ability to acquire foreign genes by LGT may have allowed the bacterium to rapidly adapt to changing plant biomass-richmore » environments.« less

Authors:
 [1];  [2];  [2];  [1];  [1];  [3];  [2];  [4];  [5];  [5];  [6];  [6];  [7];  [8];  [1];  [2]
  1. Univ. of Georgia, Athens, GA (United States). Inst. of Bioinformatics; Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology; Univ. of Georgia, Athens, GA (United States). BioEnergy Science Center
  2. Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology; Univ. of Georgia, Athens, GA (United States). BioEnergy Science Center
  3. Univ. of Georgia, Athens, GA (United States). Inst. of Bioinformatics; Univ. of Georgia, Athens, GA (United States). BioEnergy Science Center
  4. Univ. of Georgia, Athens, GA (United States). BioEnergy Science Center; Univ. of Georgia, Athens, GA (United States). Dept. of Genetics
  5. Univ. of Georgia, Athens, GA (United States). BioEnergy Science Center
  6. Univ. of Georgia, Athens, GA (United States). BioEnergy Science Center; North Carolina State Univ., Raleigh, NC (United States). Dept. of Chemical and Biomolecular Engineering
  7. Univ. of Georgia, Athens, GA (United States). Dept. of Biochemistry and Molecular Biology; Univ. of Georgia, Athens, GA (United States). Complex Carbohydrate Research Center
  8. Aix-Marseille Univ., Marseille (France); Centre National de la Recherche Scientifique (CNRS), Marseille (France). Architecture et Fonction des Macromolecules Biologiques
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1625475
Grant/Contract Number:  
AC52-06NA25396; AC02-05CH11231; AC05-00OR22725; AC52-07NA27344
Resource Type:
Accepted Manuscript
Journal Name:
Nucleic Acids Research
Additional Journal Information:
Journal Volume: 39; Journal Issue: 8; Journal ID: ISSN 0305-1048
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Biochemistry & Molecular Biology

Citation Formats

Dam, Phuongan, Kataeva, Irina, Yang, Sung-Jae, Zhou, Fengfeng, Yin, Yanbin, Chou, Wenchi, Poole, Farris L., Westpheling, Janet, Hettich, Robert, Giannone, Richard, Lewis, Derrick L., Kelly, Robert, Gilbert, Harry J., Henrissat, Bernard, Xu, Ying, and Adams, Michael W. W. Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725. United States: N. p., 2011. Web. doi:10.1093/nar/gkq1281.
Dam, Phuongan, Kataeva, Irina, Yang, Sung-Jae, Zhou, Fengfeng, Yin, Yanbin, Chou, Wenchi, Poole, Farris L., Westpheling, Janet, Hettich, Robert, Giannone, Richard, Lewis, Derrick L., Kelly, Robert, Gilbert, Harry J., Henrissat, Bernard, Xu, Ying, & Adams, Michael W. W. Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725. United States. https://doi.org/10.1093/nar/gkq1281
Dam, Phuongan, Kataeva, Irina, Yang, Sung-Jae, Zhou, Fengfeng, Yin, Yanbin, Chou, Wenchi, Poole, Farris L., Westpheling, Janet, Hettich, Robert, Giannone, Richard, Lewis, Derrick L., Kelly, Robert, Gilbert, Harry J., Henrissat, Bernard, Xu, Ying, and Adams, Michael W. W. Mon . "Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725". United States. https://doi.org/10.1093/nar/gkq1281. https://www.osti.gov/servlets/purl/1625475.
@article{osti_1625475,
title = {Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725},
author = {Dam, Phuongan and Kataeva, Irina and Yang, Sung-Jae and Zhou, Fengfeng and Yin, Yanbin and Chou, Wenchi and Poole, Farris L. and Westpheling, Janet and Hettich, Robert and Giannone, Richard and Lewis, Derrick L. and Kelly, Robert and Gilbert, Harry J. and Henrissat, Bernard and Xu, Ying and Adams, Michael W. W.},
abstractNote = {Caldicellulosiruptor bescii DSM 6725 utilizes various polysaccharides and grows efficiently on untreated high-lignin grasses and hardwood at an optimum temperature of 80C. It is a promising anaerobic bacterium for studying high-temperature biomass conversion. Its genome contains 2666 proteincoding sequences organized into 1209 operons. Expression of 2196 genes (83%) was confirmed experimentally. At least 322 genes appear to have been obtained by lateral gene transfer (LGT). Putative functions were assigned to 364 conserved/hypothetical protein (C/HP) genes. The genome contains 171 and 88 genes related to carbohydrate transport and utilization, respectively. Growth on cellulose led to the up-regulation of 32 carbohydrate-active (CAZy), 61 sugar transport, 25 transcription factor and 234 C/HP genes. Some C/HPs were overproduced on cellulose or xylan, suggesting their involvement in polysaccharide conversion. A unique feature of the genome is enrichment with genes encoding multi-modular, multi-functional CAZy proteins organized into one large cluster, the products of which are proposed to act synergistically on different components of plant cell walls and to aid the ability of C. bescii to convert plant biomass. The high duplication of CAZy domains coupled with the ability to acquire foreign genes by LGT may have allowed the bacterium to rapidly adapt to changing plant biomass-rich environments.},
doi = {10.1093/nar/gkq1281},
journal = {Nucleic Acids Research},
number = 8,
volume = 39,
place = {United States},
year = {Mon Jan 10 00:00:00 EST 2011},
month = {Mon Jan 10 00:00:00 EST 2011}
}

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  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep25279

Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times
journal, September 2018

  • Liang, Xiaoyu; Whitham, Jason M.; Holwerda, Evert K.
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1238-1

Improved growth media and culture techniques for genetic analysis and assessment of biomass utilization by Caldicellulosiruptor bescii
journal, November 2012

  • Farkas, Joel; Chung, Daehwan; Cha, Minseok
  • Journal of Industrial Microbiology & Biotechnology, Vol. 40, Issue 1, p. 41-49
  • DOI: 10.1007/s10295-012-1202-1

Genomic and secretomic insight into lignocellulolytic system of an endophytic bacterium Pantoea ananatis Sd-1
journal, February 2016


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

Insights into the roles of non-catalytic residues in the active site of a GH10 xylanase with activity on cellulose
journal, October 2017

  • Chu, Yindi; Tu, Tao; Penttinen, Leena
  • Journal of Biological Chemistry, Vol. 292, Issue 47
  • DOI: 10.1074/jbc.m117.807768

Decoding the complete arsenal for cellulose and hemicellulose deconstruction in the highly efficient cellulose decomposer Paenibacillus O199
journal, May 2016

  • López-Mondéjar, Rubén; Zühlke, Daniela; Větrovský, Tomáš
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0518-x

SGNH hydrolase-type esterase domain containing Cbes-AcXE2: a novel and thermostable acetyl xylan esterase from Caldicellulosiruptor bescii
journal, April 2017


Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems
journal, April 2016

  • López-Mondéjar, Rubén; Zühlke, Daniela; Becher, Dörte
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep25279

RNA Binding Motif Protein 48 Is Required for U12 Splicing and Maize Endosperm Differentiation
journal, February 2019

  • Bai, Fang; Corll, Jacob; Shodja, Donya N.
  • The Plant Cell, Vol. 31, Issue 3
  • DOI: 10.1105/tpc.18.00754

Single-step ethanol production from lignocellulose using novel extremely thermophilic bacteria
journal, January 2013

  • Svetlitchnyi, Vitali A.; Kensch, Oliver; Falkenhan, Doris A.
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-31

Overcoming restriction as a barrier to DNA transformation in Caldicellulosiruptor species results in efficient marker replacement
journal, January 2013

  • Chung, Daehwan; Farkas, Joel; Westpheling, Janet
  • Biotechnology for Biofuels, Vol. 6, Issue 1
  • DOI: 10.1186/1754-6834-6-82

Heterologous complementation of a pyrF deletion in Caldicellulosiruptor hydrothermalisgenerates a new host for the analysis of biomass deconstruction
journal, September 2014


Deletion of Caldicellulosiruptor besciiCelA reveals its crucial role in the deconstruction of lignocellulosic biomass
journal, October 2014

  • Young, Jenna; Chung, Daehwan; Bomble, Yannick J.
  • Biotechnology for Biofuels, Vol. 7, Issue 1
  • DOI: 10.1186/s13068-014-0142-6

Decoding the complete arsenal for cellulose and hemicellulose deconstruction in the highly efficient cellulose decomposer Paenibacillus O199
journal, May 2016

  • López-Mondéjar, Rubén; Zühlke, Daniela; Větrovský, Tomáš
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0518-x

High activity CAZyme cassette for improving biomass degradation in thermophiles
journal, February 2018

  • Brunecky, Roman; Chung, Daehwan; Sarai, Nicholas S.
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1014-2

Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times
journal, September 2018

  • Liang, Xiaoyu; Whitham, Jason M.; Holwerda, Evert K.
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1238-1

Creation of a functional hyperthermostable designer cellulosome
journal, February 2019

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

The GH10 and GH48 dual-functional catalytic domains from a multimodular glycoside hydrolase synergize in hydrolyzing both cellulose and xylan
journal, December 2019


ECOMICS: A Web-Based Toolkit for Investigating the Biomolecular Web in Ecosystems Using a Trans-omics Approach
journal, February 2012


Supplementing with Non-Glycoside Hydrolase Proteins Enhances Enzymatic Deconstruction of Plant Biomass
journal, August 2012


Methylation by a Unique α-class N4-Cytosine Methyltransferase Is Required for DNA Transformation of Caldicellulosiruptor bescii DSM6725
journal, August 2012


Design and development of synthetic microbial platform cells for bioenergy
journal, January 2013


Complete Genome Sequence of Clostridium clariflavum DSM 19732
journal, March 2012

  • Izquierdo, Javier A.; Goodwin, Lynne; Davenport, Karen W.
  • Standards in Genomic Sciences, Vol. 6, Issue 1
  • DOI: 10.4056/sigs.2535732