Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>

ABSTRACT 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 pro...

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Autores principales:	Dmitry A. Rodionov, Irina A. Rodionova, Vladimir A. Rodionov, Aleksandr A. Arzamasov, Ke Zhang, Gabriel M. Rubinstein, Tania N. N. Tanwee, Ryan G. Bing, James R. Crosby, Intawat Nookaew, Mirko Basen, Steven D. Brown, Charlotte M. Wilson, Dawn M. Klingeman, Farris L. Poole, Ying Zhang, Robert M. Kelly, Michael W. W. Adams
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Caldicellulosiruptor bescii lignocellulose degradation carbohydrate metabolism transcriptional regulation Caldicellulosiruptor carbohydrate utilization Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a6422628448b4bf5b9fbebf42000f112
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spelling	oai:doaj.org-article:a6422628448b4bf5b9fbebf42000f1122021-12-02T18:21:27ZTranscriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>10.1128/mSystems.01345-202379-5077https://doaj.org/article/a6422628448b4bf5b9fbebf42000f1122021-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01345-20https://doaj.org/toc/2379-5077ABSTRACT 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. IMPORTANCE To develop functional metabolic engineering platforms for nonmodel microorganisms, a comprehensive understanding of the physiological and metabolic characteristics is critical. Caldicellulosiruptor bescii and other species in this genus have untapped potential for conversion of unpretreated plant biomass into industrial fuels and chemicals. The highly interactive and complex machinery used by C. bescii to acquire and process complex carbohydrates contained in lignocellulose was elucidated here to complement related efforts to develop a metabolic engineering platform with this bacterium. Guided by the findings here, a clearer picture of how C. bescii natively drives carbohydrate utilization is provided and strategies to engineer this bacterium for optimal conversion of lignocellulose to commercial products emerge.Dmitry A. RodionovIrina A. RodionovaVladimir A. RodionovAleksandr A. ArzamasovKe ZhangGabriel M. RubinsteinTania N. N. TanweeRyan G. BingJames R. CrosbyIntawat NookaewMirko BasenSteven D. BrownCharlotte M. WilsonDawn M. KlingemanFarris L. PooleYing ZhangRobert M. KellyMichael W. W. AdamsAmerican Society for MicrobiologyarticleCaldicellulosiruptor besciilignocellulose degradationcarbohydrate metabolismtranscriptional regulationCaldicellulosiruptorcarbohydrate utilizationMicrobiologyQR1-502ENmSystems, Vol 6, Iss 3 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Caldicellulosiruptor bescii lignocellulose degradation carbohydrate metabolism transcriptional regulation Caldicellulosiruptor carbohydrate utilization Microbiology QR1-502
spellingShingle	Caldicellulosiruptor bescii lignocellulose degradation carbohydrate metabolism transcriptional regulation Caldicellulosiruptor carbohydrate utilization Microbiology QR1-502 Dmitry A. Rodionov Irina A. Rodionova Vladimir A. Rodionov Aleksandr A. Arzamasov Ke Zhang Gabriel M. Rubinstein Tania N. N. Tanwee Ryan G. Bing James R. Crosby Intawat Nookaew Mirko Basen Steven D. Brown Charlotte M. Wilson Dawn M. Klingeman Farris L. Poole Ying Zhang Robert M. Kelly Michael W. W. Adams Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>
description	ABSTRACT 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. IMPORTANCE To develop functional metabolic engineering platforms for nonmodel microorganisms, a comprehensive understanding of the physiological and metabolic characteristics is critical. Caldicellulosiruptor bescii and other species in this genus have untapped potential for conversion of unpretreated plant biomass into industrial fuels and chemicals. The highly interactive and complex machinery used by C. bescii to acquire and process complex carbohydrates contained in lignocellulose was elucidated here to complement related efforts to develop a metabolic engineering platform with this bacterium. Guided by the findings here, a clearer picture of how C. bescii natively drives carbohydrate utilization is provided and strategies to engineer this bacterium for optimal conversion of lignocellulose to commercial products emerge.
format	article
author	Dmitry A. Rodionov Irina A. Rodionova Vladimir A. Rodionov Aleksandr A. Arzamasov Ke Zhang Gabriel M. Rubinstein Tania N. N. Tanwee Ryan G. Bing James R. Crosby Intawat Nookaew Mirko Basen Steven D. Brown Charlotte M. Wilson Dawn M. Klingeman Farris L. Poole Ying Zhang Robert M. Kelly Michael W. W. Adams
author_facet	Dmitry A. Rodionov Irina A. Rodionova Vladimir A. Rodionov Aleksandr A. Arzamasov Ke Zhang Gabriel M. Rubinstein Tania N. N. Tanwee Ryan G. Bing James R. Crosby Intawat Nookaew Mirko Basen Steven D. Brown Charlotte M. Wilson Dawn M. Klingeman Farris L. Poole Ying Zhang Robert M. Kelly Michael W. W. Adams
author_sort	Dmitry A. Rodionov
title	Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>
title_short	Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>
title_full	Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>
title_fullStr	Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>
title_full_unstemmed	Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>
title_sort	transcriptional regulation of plant biomass degradation and carbohydrate utilization genes in the extreme thermophile <italic toggle="yes">caldicellulosiruptor bescii</italic>
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/a6422628448b4bf5b9fbebf42000f112
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Transcriptional Regulation of Plant Biomass Degradation and Carbohydrate Utilization Genes in the Extreme Thermophile <italic toggle="yes">Caldicellulosiruptor bescii</italic>

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