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Title: Genus-wide assessment of lignocellulose utilization in the extremely thermophilic Caldicellulosiruptor by genomic, pan-genomic and metagenomic analysis

Abstract

Metagenomic data from Obsidian Pool (Yellowstone National Park, USA) and thirteen genome sequences were used to re-assess genus-wide biodiversity for the extremely thermophilicCaldicellulosiruptor. The updated core-genome contains 1,401 ortholog groups (average genome size for thirteen species = 2,516 genes). The pan-genome, which remains open with a revised total of 3,493 ortholog groups, encodes a variety of multi-domain glycoside hydrolases (GH). These include three cellulases with GH48 domains that are co-located in the Glucan Degradation Locus (GDL) and are specific determinants for microcrystalline cellulose utilization. Three recently sequenced species,Caldicellulosiruptorsp. str. Rt8.B8 (re-named hereCaldicellulosiruptor morganii),Thermoanaerobacter cellulolyticusstr. NA10 (re-named hereCaldicellulosiruptor naganoensisNA10), andCaldicellulosiruptorsp. str. Wai35.B1 (re-named hereCaldicellulosiruptor danielii) degraded Avicel and lignocellulose (switchgrass).C. morganiiwas more efficient thanC. besciiin this regard and differed from the other twelve species examined here, both based on genome content and organization and in the specific domain features of conserved GHs. Metagenomic analysis of lignocellulose-enriched samples from Obsidian Pool revealed limited new information on genus biodiversity. Enrichments yielded genomic signatures closely related toCaldicellulosiruptor obsidiansis, but there was also evidence for other thermophilic fermentative anaerobes (Caldanaerobacter,Fervidobacterium,Caloramator, andClostridium). One enrichment, containing 89.7%Caldicellulosiruptorand 9.7%Caloramator, had a capacity for switchgrass solubilization comparable toC. bescii. These results refine the known biodiversity ofCaldicellulosiruptorand indicate that microcrystallinemore » cellulose degradation at temperatures above 70°C, based on current information, is limited to certain members of this genus that produce GH48 domain-containing enzymes. The genusCaldicellulosiruptorcontains the most thermophilic bacteria capable of lignocellulose deconstruction and are promising candidates for consolidated bioprocessing for the production of biofuels and bio-based chemicals. The focus here is on the extant capability of this genus for plant biomass degradation and the extent to which this can be inferred from the core and pan-genomes, based on analysis of thirteen species and metagenomic sequence information from environmental samples. Key to microcrystalline hydrolysis is the content of the Glucan Degradation Locus (GDL), a set of genes encoding glycoside hydrolases (GH), several of which have GH48 and family 3 carbohydrate binding module domains, that function as primary cellulases. Resolving the relationship between the GDL and lignocellulose degradation will inform efforts to identify more prolific members of the genus and to develop metabolic engineering strategies to improve this characteristic« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [2];  [2];  [3];  [2];  [2];  [4];  [2];  [5];  [1]
  1. North Carolina State Univ., Raleigh, NC (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of Tennessee, Knoxville, TN (United States)
  5. Univ. of Georgia, Athens, GA (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1432145
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 84; Journal Issue: n/a; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Lee, Laura L., Blumer-Schuette, Sara E., Izquierdo, Javier A., Zurawski, Jeffrey V., Loder, Andrew J., Conway, Jonathan M., Elkins, James G., Podar, Mircea, Clum, Alicia, Jones, Piet C., Piatek, Marek J., Weighill, Deborah A., Jacobson, Daniel A., Adams, Michael W. W., and Kelly, Robert M. Genus-wide assessment of lignocellulose utilization in the extremely thermophilic Caldicellulosiruptor by genomic, pan-genomic and metagenomic analysis. United States: N. p., 2018. Web. doi:10.1128/AEM.02694-17.
Lee, Laura L., Blumer-Schuette, Sara E., Izquierdo, Javier A., Zurawski, Jeffrey V., Loder, Andrew J., Conway, Jonathan M., Elkins, James G., Podar, Mircea, Clum, Alicia, Jones, Piet C., Piatek, Marek J., Weighill, Deborah A., Jacobson, Daniel A., Adams, Michael W. W., & Kelly, Robert M. Genus-wide assessment of lignocellulose utilization in the extremely thermophilic Caldicellulosiruptor by genomic, pan-genomic and metagenomic analysis. United States. doi:10.1128/AEM.02694-17.
Lee, Laura L., Blumer-Schuette, Sara E., Izquierdo, Javier A., Zurawski, Jeffrey V., Loder, Andrew J., Conway, Jonathan M., Elkins, James G., Podar, Mircea, Clum, Alicia, Jones, Piet C., Piatek, Marek J., Weighill, Deborah A., Jacobson, Daniel A., Adams, Michael W. W., and Kelly, Robert M. Fri . "Genus-wide assessment of lignocellulose utilization in the extremely thermophilic Caldicellulosiruptor by genomic, pan-genomic and metagenomic analysis". United States. doi:10.1128/AEM.02694-17. https://www.osti.gov/servlets/purl/1432145.
@article{osti_1432145,
title = {Genus-wide assessment of lignocellulose utilization in the extremely thermophilic Caldicellulosiruptor by genomic, pan-genomic and metagenomic analysis},
author = {Lee, Laura L. and Blumer-Schuette, Sara E. and Izquierdo, Javier A. and Zurawski, Jeffrey V. and Loder, Andrew J. and Conway, Jonathan M. and Elkins, James G. and Podar, Mircea and Clum, Alicia and Jones, Piet C. and Piatek, Marek J. and Weighill, Deborah A. and Jacobson, Daniel A. and Adams, Michael W. W. and Kelly, Robert M.},
abstractNote = {Metagenomic data from Obsidian Pool (Yellowstone National Park, USA) and thirteen genome sequences were used to re-assess genus-wide biodiversity for the extremely thermophilicCaldicellulosiruptor. The updated core-genome contains 1,401 ortholog groups (average genome size for thirteen species = 2,516 genes). The pan-genome, which remains open with a revised total of 3,493 ortholog groups, encodes a variety of multi-domain glycoside hydrolases (GH). These include three cellulases with GH48 domains that are co-located in the Glucan Degradation Locus (GDL) and are specific determinants for microcrystalline cellulose utilization. Three recently sequenced species,Caldicellulosiruptorsp. str. Rt8.B8 (re-named hereCaldicellulosiruptor morganii),Thermoanaerobacter cellulolyticusstr. NA10 (re-named hereCaldicellulosiruptor naganoensisNA10), andCaldicellulosiruptorsp. str. Wai35.B1 (re-named hereCaldicellulosiruptor danielii) degraded Avicel and lignocellulose (switchgrass).C. morganiiwas more efficient thanC. besciiin this regard and differed from the other twelve species examined here, both based on genome content and organization and in the specific domain features of conserved GHs. Metagenomic analysis of lignocellulose-enriched samples from Obsidian Pool revealed limited new information on genus biodiversity. Enrichments yielded genomic signatures closely related toCaldicellulosiruptor obsidiansis, but there was also evidence for other thermophilic fermentative anaerobes (Caldanaerobacter,Fervidobacterium,Caloramator, andClostridium). One enrichment, containing 89.7%Caldicellulosiruptorand 9.7%Caloramator, had a capacity for switchgrass solubilization comparable toC. bescii. These results refine the known biodiversity ofCaldicellulosiruptorand indicate that microcrystalline cellulose degradation at temperatures above 70°C, based on current information, is limited to certain members of this genus that produce GH48 domain-containing enzymes. The genusCaldicellulosiruptorcontains the most thermophilic bacteria capable of lignocellulose deconstruction and are promising candidates for consolidated bioprocessing for the production of biofuels and bio-based chemicals. The focus here is on the extant capability of this genus for plant biomass degradation and the extent to which this can be inferred from the core and pan-genomes, based on analysis of thirteen species and metagenomic sequence information from environmental samples. Key to microcrystalline hydrolysis is the content of the Glucan Degradation Locus (GDL), a set of genes encoding glycoside hydrolases (GH), several of which have GH48 and family 3 carbohydrate binding module domains, that function as primary cellulases. Resolving the relationship between the GDL and lignocellulose degradation will inform efforts to identify more prolific members of the genus and to develop metabolic engineering strategies to improve this characteristic},
doi = {10.1128/AEM.02694-17},
journal = {Applied and Environmental Microbiology},
number = n/a,
volume = 84,
place = {United States},
year = {2018},
month = {2}
}

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    Works referencing / citing this record:

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