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Title: Genome and Transcriptome of Clostridium phytofermentans, Catalyst for the Direct Conversion of Plant Feedstocks to Fuels

Abstract

Clostridium phytofermentans was isolated from forest soil and is distinguished by its capacity to directly ferment plant cell wall polysaccharides into ethanol as the primary product, suggesting that it possesses unusual catabolic pathways. In this paper, the objective of the present study was to understand the molecular mechanisms of biomass conversion to ethanol in a single organism, Clostridium phytofermentans, by analyzing its complete genome and transcriptome during growth on plant carbohydrates. The saccharolytic versatility of C. phytofermentans is reflected in a diversity of genes encoding ATP-binding cassette sugar transporters and glycoside hydrolases, many of which may have been acquired through horizontal gene transfer. These genes are frequently organized as operons that may be controlled individually by the many transcriptional regulators identified in the genome. Preferential ethanol production may be due to high levels of expression of multiple ethanol dehydrogenases and additional pathways maximizing ethanol yield. The genome also encodes three different proteinaceous bacterial microcompartments with the capacity to compartmentalize pathways that divert fermentation intermediates to various products. Finally, these characteristics make C. phytofermentans an attractive resource for improving the efficiency and speed of biomass conversion to biofuels.

Authors:
 [1];  [1];  [2];  [3];  [1];  [4];  [1];  [4];  [4];  [5];  [5];  [6];  [6];  [5];  [7];  [1];  [8];  [9];  [10];  [11]
  1. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology
  2. Univ. of Massachusetts, Amherst, MA (United States). Graduate Program in Molecular and Cellular Biology; Univ. of Massachusetts, Amherst, MA (United States). Inst. for Cellular Engineering
  3. National Center for Scientific Research (CNRS), Evry (France). Alternative Energies and Atomic Energy Commission (CEA)-Genoscope. Mixed Research Unit (UMR)-8030
  4. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology; Univ. of Massachusetts, Amherst, MA (United States). Inst. for Cellular Engineering
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States). Genome Biology Program. Production Genomics Facility
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Life Sciences Division
  7. Aix-Marseille Univ. I and II, Marseille (France). National Center for Scientific Research (CNRS). Architecture and Function of Biological Macromolecules. Mixed Research Unit (UMR)-6098
  8. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Biochemistry and Molecular Biology
  9. Harvard Medical School, Boston, MA (United States). Dept. of Genetics
  10. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology; Univ. of Massachusetts, Amherst, MA (United States). Inst. for Cellular Engineering; Univ. of Massachusetts, Amherst, MA (United States). Dept. of Veterinary and Animal Sciences
  11. Univ. of Massachusetts, Amherst, MA (United States). Dept. of Microbiology; Univ. of Massachusetts, Amherst, MA (United States). Graduate Program in Molecular and Cellular Biology; Univ. of Massachusetts, Amherst, MA (United States). Inst. for Cellular Engineering; Univ. of Massachusetts, Amherst, MA (United States). Graduate Program in Organismal and Evolutionary Biology; Univ. of Massachusetts, Amherst, MA (United States). Dept. of Biology
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States); Oak Ridge Y-12 Plant (Y-12), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
Contributing Org.:
Univ. of Massachusetts, Amherst, MA (United States)
OSTI Identifier:
1265527
Alternate Identifier(s):
OSTI ID: 1260614
Grant/Contract Number:  
AC02-05CH11231; FG02-02ER15330; FG02-02ER1533; 0722802
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 10; Journal Issue: 6; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; clostridium; ethanol; genomic databases; cellulose; gene regulation; database searching; fermentation; microarrays

Citation Formats

Petit, Elsa, Coppi, Maddalena V., Hayes, James C., Tolonen, Andrew C., Warnick, Thomas, Latouf, William G., Amisano, Danielle, Biddle, Amy, Mukherjee, Supratim, Ivanova, Natalia, Lykidis, Athanassios, Land, Miriam, Hauser, Loren, Kyrpides, Nikos, Henrissat, Bernard, Lau, Joanne, Schnell, Danny J., Church, George M., Leschine, Susan B., and Blanchard, Jeffrey L. Genome and Transcriptome of Clostridium phytofermentans, Catalyst for the Direct Conversion of Plant Feedstocks to Fuels. United States: N. p., 2015. Web. doi:10.1371/journal.pone.0118285.
Petit, Elsa, Coppi, Maddalena V., Hayes, James C., Tolonen, Andrew C., Warnick, Thomas, Latouf, William G., Amisano, Danielle, Biddle, Amy, Mukherjee, Supratim, Ivanova, Natalia, Lykidis, Athanassios, Land, Miriam, Hauser, Loren, Kyrpides, Nikos, Henrissat, Bernard, Lau, Joanne, Schnell, Danny J., Church, George M., Leschine, Susan B., & Blanchard, Jeffrey L. Genome and Transcriptome of Clostridium phytofermentans, Catalyst for the Direct Conversion of Plant Feedstocks to Fuels. United States. https://doi.org/10.1371/journal.pone.0118285
Petit, Elsa, Coppi, Maddalena V., Hayes, James C., Tolonen, Andrew C., Warnick, Thomas, Latouf, William G., Amisano, Danielle, Biddle, Amy, Mukherjee, Supratim, Ivanova, Natalia, Lykidis, Athanassios, Land, Miriam, Hauser, Loren, Kyrpides, Nikos, Henrissat, Bernard, Lau, Joanne, Schnell, Danny J., Church, George M., Leschine, Susan B., and Blanchard, Jeffrey L. Tue . "Genome and Transcriptome of Clostridium phytofermentans, Catalyst for the Direct Conversion of Plant Feedstocks to Fuels". United States. https://doi.org/10.1371/journal.pone.0118285. https://www.osti.gov/servlets/purl/1265527.
@article{osti_1265527,
title = {Genome and Transcriptome of Clostridium phytofermentans, Catalyst for the Direct Conversion of Plant Feedstocks to Fuels},
author = {Petit, Elsa and Coppi, Maddalena V. and Hayes, James C. and Tolonen, Andrew C. and Warnick, Thomas and Latouf, William G. and Amisano, Danielle and Biddle, Amy and Mukherjee, Supratim and Ivanova, Natalia and Lykidis, Athanassios and Land, Miriam and Hauser, Loren and Kyrpides, Nikos and Henrissat, Bernard and Lau, Joanne and Schnell, Danny J. and Church, George M. and Leschine, Susan B. and Blanchard, Jeffrey L.},
abstractNote = {Clostridium phytofermentans was isolated from forest soil and is distinguished by its capacity to directly ferment plant cell wall polysaccharides into ethanol as the primary product, suggesting that it possesses unusual catabolic pathways. In this paper, the objective of the present study was to understand the molecular mechanisms of biomass conversion to ethanol in a single organism, Clostridium phytofermentans, by analyzing its complete genome and transcriptome during growth on plant carbohydrates. The saccharolytic versatility of C. phytofermentans is reflected in a diversity of genes encoding ATP-binding cassette sugar transporters and glycoside hydrolases, many of which may have been acquired through horizontal gene transfer. These genes are frequently organized as operons that may be controlled individually by the many transcriptional regulators identified in the genome. Preferential ethanol production may be due to high levels of expression of multiple ethanol dehydrogenases and additional pathways maximizing ethanol yield. The genome also encodes three different proteinaceous bacterial microcompartments with the capacity to compartmentalize pathways that divert fermentation intermediates to various products. Finally, these characteristics make C. phytofermentans an attractive resource for improving the efficiency and speed of biomass conversion to biofuels.},
doi = {10.1371/journal.pone.0118285},
journal = {PLoS ONE},
number = 6,
volume = 10,
place = {United States},
year = {Tue Jun 02 00:00:00 EDT 2015},
month = {Tue Jun 02 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 16 works
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Figures / Tables:

Figure 1 Figure 1: Neighbor-joining tree of C. phytofermentans and related taxa within the class Clostridia based on 16S rRNA gene sequences. Taxa with sequenced genomes are marked with an asterisk. Cluster numbers correspond to the cluster system of Collins et al. Bootstrap values were determined for 1,000 replicates.

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Domesticated equine species and their derived hybrids differ in their fecal microbiota
journal, March 2020


Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring
journal, March 2017

  • Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0756-6

Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring
journal, March 2017

  • Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0756-6

The Hybrid Strategy of Thermoactinospora rubra YIM 77501T for Utilizing Cellulose as a Carbon Source at Different Temperatures
journal, May 2017


Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.