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Title: Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile Caldicellulosiruptor bescii

Journal Article · · mSystems
ORCiD logo [1]; ORCiD logo [2];  [3];  [1];  [4];  [5];  [5];  [6];  [6];  [7]; ORCiD logo [8];  [9];  [10];  [9];  [5]; ORCiD logo [4];  [6]; ORCiD logo [5];
  1. Sanford-Burnhams-Prebys Medical Discovery Institute, La Jolla, California, USA, A.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  2. Department of Bioengineering, University of California—San Diego, La Jolla, California, USA
  3. A.A. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  4. Department of Cell and Molecular Biology, College of the Environment and Life Sciences, University of Rhode Island, Kingston, Rhode Island, USA
  5. Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, USA
  6. Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, North Carolina, USA
  7. Department of Biomedical Informatics, College of Medicine, University of Arkansas for Medical Sciences, Little Rock, Arkansas, USA, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
  8. Mathematisch-Naturwissenschaftliche Fakultät, Institut für Biowissenschaften, Mikrobiologie, Universität Rostock, Rostock, Germany
  9. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
  10. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA, University of Otago, Dunedin, New Zealand

Extremely thermophilic bacteria from the genus Caldicellulosiruptor can degrade polysaccharide components of plant cell walls and subsequently utilize the constituting mono- and oligosaccharides. Through metabolic engineering, ethanol and other industrially important end products can be produced. Previous experimental studies identified a variety of carbohydrate-active enzymes in model species Caldicellulosiruptor saccharolyticus and Caldicellulosiruptor bescii, while prior transcriptomic experiments identified their putative carbohydrate uptake transporters. We investigated the mechanisms of transcriptional regulation of carbohydrate utilization genes using a comparative genomics approach applied to 14 Caldicellulosiruptor species. The reconstruction of carbohydrate utilization regulatory network includes the predicted binding sites for 34 mostly local regulators and point to the regulatory mechanisms controlling expression of genes involved in degradation of plant biomass. The Rex and CggR regulons control the central glycolytic and primary redox reactions. The identified transcription factor binding sites and regulons were validated with transcriptomic and transcription start site experimental data for C. bescii grown on cellulose, cellobiose, glucose, xylan, and xylose. The XylR and XynR regulons control xylan-induced transcriptional response of genes involved in degradation of xylan and xylose utilization. The reconstructed regulons informed the carbohydrate utilization reconstruction analysis and improved functional annotations of 51 transporters and 11 catabolic enzymes. Using gene deletion, we confirmed that the shared ATPase component MsmK is essential for growth on oligo- and polysaccharides but not for the utilization of monosaccharides. By elucidating the carbohydrate utilization framework in C. bescii, strategies for metabolic engineering can be pursued to optimize yields of bio-based fuels and chemicals from lignocellulose.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health(NIH)
Grant/Contract Number:
SC0019391; AC05-00OR22725; P20GM125503
OSTI ID:
1787883
Alternate ID(s):
OSTI ID: 1819549
Journal Information:
mSystems, Journal Name: mSystems Vol. 6 Journal Issue: 3; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

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