Genus-wide assessment of lignocellulose utilization in the extremely thermophilic genus Caldicellulosiruptor by genomic, pangenomic, and metagenomic analyses

Laura L. Lee; Sara E. Blumer-Schuette; Javier A. Izquierdo; Jeffrey V. Zurawski; Andrew J. Loder; Jonathan M. Conway; James G. Elkins; Mircea Podar; Alicia Clum; Piet C. Jones; Marek J. Piatek; Deborah A. Weighill; Daniel A. Jacobson; Michael W.W. Adams; Robert M. Kelly

doi:10.1128/AEM.02694-17

Genus-wide assessment of lignocellulose utilization in the extremely thermophilic genus Caldicellulosiruptor by genomic, pangenomic, and metagenomic analyses

Laura L. Lee, Sara E. Blumer-Schuette, Javier A. Izquierdo, Jeffrey V. Zurawski, Andrew J. Loder, Jonathan M. Conway, James G. Elkins, Mircea Podar, Alicia Clum, Piet C. Jones, Marek J. Piatek, Deborah A. Weighill, Daniel A. Jacobson, Michael W.W. Adams, Robert M. Kelly

Research output: Contribution to journal › Article › peer-review

31 Scopus citations

Abstract

Metagenomic data from Obsidian Pool (Yellowstone National Park, USA) and 13 genome sequences were used to reassess genus-wide biodiversity for the extremely thermophilic Caldicellulosiruptor. The updated core genome contains 1,401 ortholog groups (average genome size for 13 species = 2,516 genes). The pangenome, which remains open with a revised total of 3,493 ortholog groups, encodes a variety of multidomain glycoside hydrolases (GHs). These include three cellulases with GH48 domains that are colocated in the glucan degradation locus (GDL) and are specific determinants for microcrystalline cellulose utilization. Three recently sequenced species, Caldicellulosiruptor sp. strain Rt8.B8 (renamed here Caldicellulosiruptor morganii), Thermoanaerobacter cellulolyticus strain NA10 (renamed here Caldicellulosiruptor naganoensis), and Caldicellulosiruptor sp. strain Wai35.B1 (renamed here Caldicellulosiruptor danielii), degraded Avicel and lignocellulose (switchgrass). C. morganii was more efficient than Caldicellulosiruptor bescii in this regard and differed from the other 12 species examined, 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 to that of Caldicellulosiruptor obsidiansis, but there was also evidence for other thermophilic fermentative anaerobes (Caldanaerobacter, Fervidobacterium, Caloramator, and Clostridium). One enrichment, containing 89.8% Caldicellulosiruptor and 9.7% Caloramator, had a capacity for switchgrass solubilization comparable to that of C. bescii. These results refine the known biodiversity of Caldicellulosiruptor and 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.

Original language	English
Article number	e02694-17
Journal	Applied and Environmental Microbiology
Volume	84
Issue number	9
DOIs	https://doi.org/10.1128/AEM.02694-17
State	Published - May 1 2018

Funding

This work was supported by the BioEnergy Science Center (BESC), a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. L. L. Lee acknowledges support from a National Science Foundation Graduate Research Fellowship and an NIH T32 Biotechnology Traineeship (GM008776-11). J. M. Conway acknowledges support from a U.S. DoEd GAANN fellowship (P200A100004-12). A. J. Loder acknowledges support from an NIH T32 biotechnology traineeship (GM008776-11). We acknowledge the help of Bernard Henrissat, AFMB University-Marseille, for characterizing CAZyme families in new members of the genus Caldicellulosiruptor. Metagenomic sequencing and analysis were conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science user facility which is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231. This research also used resources of the Oak Ridge Leadership Computing Facility and the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory. We also thank the administration of the Yellowstone National Park Service for coordinating sample collection within YNP under permit number YELL-2012-SCI-5714 and Christie L. Hendrix and Stacey Gunther for coordinating sampling activities

Funders	Funder number
AFMB University-Marseille
Bernard Henrissat
BioEnergy Science Center
CADES
Data Environment for Science
U.S. Department of Energy Bioenergy Research Center
U.S. Department of Energy Joint Genome Institute
Yellowstone National Park Service	YELL-2012-SCI-5714
National Science Foundation
National Institutes of Health	P200A100004-12
U.S. Department of Energy	DE-AC02-05CH11231
National Institute of General Medical Sciences	T32GM008776
Office of Science
Biological and Environmental Research
Oak Ridge National Laboratory

Keywords

Caldicellulosiruptor
Extreme thermophile
Pangenome

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10.1128/AEM.02694-17

Cite this

Lee, L. L., Blumer-Schuette, S. E., Izquierdo, J. A., Zurawski, J. V., Loder, A. J., Conway, J. M., Elkins, J. G., Podar, M., Clum, A., Jones, P. C., Piatek, M. J., Weighill, D. A., Jacobson, D. A., Adams, M. W. W., & Kelly, R. M. (2018). Genus-wide assessment of lignocellulose utilization in the extremely thermophilic genus Caldicellulosiruptor by genomic, pangenomic, and metagenomic analyses. Applied and Environmental Microbiology, 84(9), Article e02694-17. https://doi.org/10.1128/AEM.02694-17

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abstract = "Metagenomic data from Obsidian Pool (Yellowstone National Park, USA) and 13 genome sequences were used to reassess genus-wide biodiversity for the extremely thermophilic Caldicellulosiruptor. The updated core genome contains 1,401 ortholog groups (average genome size for 13 species = 2,516 genes). The pangenome, which remains open with a revised total of 3,493 ortholog groups, encodes a variety of multidomain glycoside hydrolases (GHs). These include three cellulases with GH48 domains that are colocated in the glucan degradation locus (GDL) and are specific determinants for microcrystalline cellulose utilization. Three recently sequenced species, Caldicellulosiruptor sp. strain Rt8.B8 (renamed here Caldicellulosiruptor morganii), Thermoanaerobacter cellulolyticus strain NA10 (renamed here Caldicellulosiruptor naganoensis), and Caldicellulosiruptor sp. strain Wai35.B1 (renamed here Caldicellulosiruptor danielii), degraded Avicel and lignocellulose (switchgrass). C. morganii was more efficient than Caldicellulosiruptor bescii in this regard and differed from the other 12 species examined, 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 to that of Caldicellulosiruptor obsidiansis, but there was also evidence for other thermophilic fermentative anaerobes (Caldanaerobacter, Fervidobacterium, Caloramator, and Clostridium). One enrichment, containing 89.8% Caldicellulosiruptor and 9.7% Caloramator, had a capacity for switchgrass solubilization comparable to that of C. bescii. These results refine the known biodiversity of Caldicellulosiruptor and 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.",

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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 Mircea Podar and Alicia Clum 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.}",

note = "Publisher Copyright: {\textcopyright} 2018 American Society for Microbiology.",

year = "2018",

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doi = "10.1128/AEM.02694-17",

language = "English",

volume = "84",

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Lee, LL, Blumer-Schuette, SE, Izquierdo, JA, Zurawski, JV, Loder, AJ, Conway, JM, Elkins, JG, Podar, M, Clum, A, Jones, PC, Piatek, MJ, Weighill, DA, Jacobson, DA, Adams, MWW & Kelly, RM 2018, 'Genus-wide assessment of lignocellulose utilization in the extremely thermophilic genus Caldicellulosiruptor by genomic, pangenomic, and metagenomic analyses', Applied and Environmental Microbiology, vol. 84, no. 9, e02694-17. https://doi.org/10.1128/AEM.02694-17

Genus-wide assessment of lignocellulose utilization in the extremely thermophilic genus Caldicellulosiruptor by genomic, pangenomic, and metagenomic analyses. / Lee, Laura L.; Blumer-Schuette, Sara E.; Izquierdo, Javier A. et al.
In: Applied and Environmental Microbiology, Vol. 84, No. 9, e02694-17, 01.05.2018.

Research output: Contribution to journal › Article › peer-review

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AU - Lee, Laura L.

AU - Blumer-Schuette, Sara E.

AU - Izquierdo, Javier A.

AU - Zurawski, Jeffrey V.

AU - Loder, Andrew J.

AU - Conway, Jonathan M.

AU - Elkins, James G.

AU - Podar, Mircea

AU - Clum, Alicia

AU - Jones, Piet C.

AU - Piatek, Marek J.

AU - Weighill, Deborah A.

AU - Jacobson, Daniel A.

AU - Adams, Michael W.W.

AU - Kelly, Robert M.

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AB - Metagenomic data from Obsidian Pool (Yellowstone National Park, USA) and 13 genome sequences were used to reassess genus-wide biodiversity for the extremely thermophilic Caldicellulosiruptor. The updated core genome contains 1,401 ortholog groups (average genome size for 13 species = 2,516 genes). The pangenome, which remains open with a revised total of 3,493 ortholog groups, encodes a variety of multidomain glycoside hydrolases (GHs). These include three cellulases with GH48 domains that are colocated in the glucan degradation locus (GDL) and are specific determinants for microcrystalline cellulose utilization. Three recently sequenced species, Caldicellulosiruptor sp. strain Rt8.B8 (renamed here Caldicellulosiruptor morganii), Thermoanaerobacter cellulolyticus strain NA10 (renamed here Caldicellulosiruptor naganoensis), and Caldicellulosiruptor sp. strain Wai35.B1 (renamed here Caldicellulosiruptor danielii), degraded Avicel and lignocellulose (switchgrass). C. morganii was more efficient than Caldicellulosiruptor bescii in this regard and differed from the other 12 species examined, 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 to that of Caldicellulosiruptor obsidiansis, but there was also evidence for other thermophilic fermentative anaerobes (Caldanaerobacter, Fervidobacterium, Caloramator, and Clostridium). One enrichment, containing 89.8% Caldicellulosiruptor and 9.7% Caloramator, had a capacity for switchgrass solubilization comparable to that of C. bescii. These results refine the known biodiversity of Caldicellulosiruptor and 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.

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Genus-wide assessment of lignocellulose utilization in the extremely thermophilic genus Caldicellulosiruptor by genomic, pangenomic, and metagenomic analyses

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