Quantitative fermentation of unpretreated transgenic poplar by Caldicellulosiruptor bescii

Straub, Christopher T.; Khatibi, Piyum A.; Wang, Jack P.; Conway, Jonathan M.; Williams-Rhaesa, Amanda M.; Peszlen, Ilona M.; Chiang, Vincent L.; Adams, Michael W.  W.; Kelly, Robert M.

doi:10.1038/s41467-019-11376-6

Title: Quantitative fermentation of unpretreated transgenic poplar by Caldicellulosiruptor bescii

Journal Article · 07 August 2019 · Nature Communications

DOI: https://doi.org/10.1038/s41467-019-11376-6 · OSTI ID:1613208

Straub, Christopher T. ^[1];

^[1]; Wang, Jack P. ^[1];

^[1];

^[2];

^[1]; Chiang, Vincent L. ^[1]; Adams, Michael W. W. ^[2];

^[1]

North Carolina State Univ., Raleigh, NC (United States)
Univ. of Georgia, Athens, GA (United States)

Microbial fermentation of lignocellulosic biomass to produce industrial chemicals is exacerbated by the recalcitrant network of lignin, cellulose and hemicelluloses comprising the plant secondary cell wall. In this study, we show that transgenic poplar (Populus trichocarpa) lines can be solubilized without any pretreatment by the extreme thermophile Caldicellulosiruptor bescii that has been metabolically engineered to shift its fermentation products away from inhibitory organic acids to ethanol. Carbohydrate solubilization and conversion of unpretreated milled biomass is nearly 90% for two transgenic lines, compared to only 25% for wild-type poplar. Unexpectedly, unpretreated intact poplar stems achieved nearly 70% of the fermentation production observed with milled poplar as the substrate. The nearly quantitative microbial conversion of the carbohydrate content of unpretreated transgenic lignocellulosic biomass bodes well for full utilization of renewable biomass feedstocks.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0019391

OSTI ID:: 1613208

Journal Information:: Nature Communications, Vol. 10, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (22)

Genome Stability in Engineered Strains of the Extremely Thermophilic Lignocellulose-Degrading Bacterium Caldicellulosiruptor bescii Williams-Rhaesa, Amanda M.; Poole, Farris L.; Dinsmore, Jessica T. Applied and Environmental Microbiology, Vol. 83, Issue 14 https://doi.org/10.1128/AEM.00444-17	journal	May 2017
Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis Wang, Jack P.; Matthews, Megan L.; Williams, Cranos M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03863-z	journal	April 2018
Thermophilic lignocellulose deconstruction Blumer-Schuette, Sara E.; Brown, Steven D.; Sander, Kyle B. FEMS Microbiology Reviews, Vol. 38, Issue 3 https://doi.org/10.1111/1574-6976.12044	journal	May 2014
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. Applied and Environmental Microbiology, Vol. 84, Issue 9 https://doi.org/10.1128/AEM.02694-17	journal	February 2018
A Highly Thermostable Kanamycin Resistance Marker Expands the Tool Kit for Genetic Manipulation of Caldicellulosiruptor bescii Lipscomb, Gina L.; Conway, Jonathan M.; Blumer-Schuette, Sara E. Applied and Environmental Microbiology, Vol. 82, Issue 14 https://doi.org/10.1128/AEM.00570-16	journal	May 2016
Multiple levers for overcoming the recalcitrance of lignocellulosic biomass Holwerda, Evert K.; Worthen, Robert S.; Kothari, Ninad Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1353-7	journal	January 2019
Natural genetic variability reduces recalcitrance in poplar Bhagia, Samarthya; Muchero, Wellington; Kumar, Rajeev Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0521-2	journal	May 2016
Woody biomass pretreatment for cellulosic ethanol production: Technology and energy consumption evaluation☆ Zhu, J. Y.; Pan, X. J. Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2009.11.007	journal	July 2010
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808 https://doi.org/10.1073/pnas.1100310108	journal	February 2011
Bioavailability of Carbohydrate Content in Natural and Transgenic Switchgrasses for the Extreme Thermophile Caldicellulosiruptor bescii Zurawski, Jeffrey V.; Khatibi, Piyum A.; Akinosho, Hannah O. Applied and Environmental Microbiology, Vol. 83, Issue 17 https://doi.org/10.1128/AEM.00969-17	journal	June 2017
Cellulose and lignin colocalization at the plant cell wall surface limits microbial hydrolysis of Populus biomass Dumitrache, Alexandru; Tolbert, Allison; Natzke, Jace Green Chemistry, Vol. 19, Issue 9 https://doi.org/10.1039/C7GC00346C	journal	January 2017
Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii Chung, D.; Cha, M.; Guss, A. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 24, p. 8931-8936 https://doi.org/10.1073/pnas.1402210111	journal	June 2014
Caldicellulosiruptor Core and Pangenomes Reveal Determinants for Noncellulosomal Thermophilic Deconstruction of Plant Biomass Blumer-Schuette, S. E.; Giannone, R. J.; Zurawski, J. V. Journal of Bacteriology, Vol. 194, Issue 15 https://doi.org/10.1128/JB.00266-12	journal	May 2012
Engineering redox-balanced ethanol production in the cellulolytic and extremely thermophilic bacterium, Caldicellulosiruptor bescii Williams-Rhaesa, Amanda M.; Rubinstein, Gabriel M.; Scott, Israel M. Metabolic Engineering Communications, Vol. 7 https://doi.org/10.1016/j.mec.2018.e00073	journal	December 2018
Complete Proteomic-Based Enzyme Reaction and Inhibition Kinetics Reveal How Monolignol Biosynthetic Enzyme Families Affect Metabolic Flux and Lignin in Populus trichocarpa Wang, Jack P.; Naik, Punith P.; Chen, Hsi-Chuan The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.120881	journal	March 2014
Woody biomass pretreatment for cellulosic ethanol production: Technology and energy consumption evaluation☆ Zhu, J. Y.; Pan, X. J. Bioresource Technology, Vol. 101, Issue 13 https://doi.org/10.1016/j.biortech.2009.11.007	journal	July 2010
Improving wood properties for wood utilization through multi-omics integration in lignin biosynthesis Wang, Jack P.; Matthews, Megan L.; Williams, Cranos M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03863-z	journal	April 2018
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808 https://doi.org/10.1073/pnas.1100310108	journal	February 2011
Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii Chung, D.; Cha, M.; Guss, A. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 24, p. 8931-8936 https://doi.org/10.1073/pnas.1402210111	journal	June 2014
Complete Proteomic-Based Enzyme Reaction and Inhibition Kinetics Reveal How Monolignol Biosynthetic Enzyme Families Affect Metabolic Flux and Lignin in Populus trichocarpa Wang, Jack P.; Naik, Punith P.; Chen, Hsi-Chuan The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.120881	journal	March 2014
Thermophilic lignocellulose deconstruction Blumer-Schuette, Sara E.; Brown, Steven D.; Sander, Kyle B. FEMS Microbiology Reviews, Vol. 38, Issue 3 https://doi.org/10.1111/1574-6976.12044	journal	May 2014
Multiple levers for overcoming the recalcitrance of lignocellulosic biomass Holwerda, Evert K.; Worthen, Robert S.; Kothari, Ninad Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1353-7	journal	January 2019

Cited By (2)

Use of the lignocellulose-degrading bacterium Caldicellulosiruptor bescii to assess recalcitrance and conversion of wild-type and transgenic poplar Straub, Christopher T.; Bing, Ryan G.; Wang, Jack P. Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01675-2	journal	March 2020
Additional file 2 of Low-abundance populations distinguish microbiome performance in plant cell wall deconstruction Tom, Lauren M.; Aulitto, Martina; Wu, Yu-Wei figshare https://doi.org/10.6084/m9.figshare.21391677	dataset	January 2022

Similar Records

Use of the lignocellulose-degrading bacterium Caldicellulosiruptor bescii to assess recalcitrance and conversion of wild-type and transgenic poplar

Journal Article · 2020 · Biotechnology for Biofuels · OSTI ID:1618775

None, None

Plant biomass fermentation by the extreme thermophile Caldicellulosiruptor bescii for co-production of green hydrogen and acetone: Technoeconomic analysis

Journal Article · 2022 · Bioresource Technology · OSTI ID:1976891

Bing, Ryan G.; Straub, Christopher T.; Sulis, Daniel B.; +3 more

Bioavailability of Carbohydrate Content in Natural and Transgenic Switchgrasses for the Extreme Thermophile Caldicellulosiruptor bescii

Journal Article · 2017 · Applied and Environmental Microbiology · OSTI ID:1394607

Zurawski, Jeffrey V.; Khatibi, Piyum A.; Akinosho, Hannah O.; +8 more

Related Subjects

09 BIOMASS FUELS
Science & Technology

Title: Quantitative fermentation of unpretreated transgenic poplar by Caldicellulosiruptor bescii

Citation Formats

References (22)

Cited By (2)

Similar Records

Related Subjects