Expression of the Acidothermus cellulolyticus E1 endoglucanase in Caldicellulosiruptor bescii enhances its ability to deconstruct crystalline cellulose

Chung, Daehwan; Young, Jenna; Cha, Minseok; Brunecky, Roman; Bomble, Yannick J.; Himmel, Michael E.; Westpheling, Janet

doi:10.1186/s13068-015-0296-x

Title: Expression of the Acidothermus cellulolyticus E1 endoglucanase in Caldicellulosiruptor bescii enhances its ability to deconstruct crystalline cellulose

Abstract

The Caldicellulosiruptor bescii genome encodes a potent set of carbohydrate-active enzymes (CAZymes), found primarily as multi-domain enzymes that exhibit high cellulolytic and hemicellulolytic activity on and allow utilization of a broad range of substrates, including plant biomass without conventional pretreatment. CelA, the most abundant cellulase in the C. bescii secretome, uniquely combines a GH9 endoglucanase and a GH48 exoglucanase in one protein. The most effective commercial enzyme cocktails used in vitro to pretreat biomass are derived from fungal cellulases (cellobiohydrolases, endoglucanases and a β-d-glucosidases) that act synergistically to release sugars for microbial conversion. The C. bescii genome contains six GH5 domains in five different open reading frames. Four exist in multi-domain proteins and two as single catalytic domains. E1 is a GH5 endoglucanase reported to have high specific activity and simple architecture and is active at the growth temperature of C. bescii. E1 is an endo-1,4-β-glucanase linked to a family 2 carbohydrate-binding module shown to bind primarily to cellulosic substrates. As a result, we tested if the addition of this protein to the C. bescii secretome would improve its cellulolytic activity.

Authors:

Chung, Daehwan ^[1]; Young, Jenna ^[1]; Cha, Minseok ^[1]; Brunecky, Roman ^[2]; Bomble, Yannick J. ^[2]; Himmel, Michael E. ^[2]; Westpheling, Janet ^[1]

Univ. of Georgia, Athens, GA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
National Renewable Energy Lab. (NREL), Golden, CO (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Publication Date:: Thu Aug 13 00:00:00 EDT 2015

Research Org.:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1225358

Report Number(s):: NREL/JA-2700-65047
Journal ID: ISSN 1754-6834

Grant/Contract Number:: AC36-08GO28308

Resource Type:: Journal Article: Accepted Manuscript

Journal Name:: Biotechnology for Biofuels

Additional Journal Information:: Journal Volume: 8; Journal Issue: 1; Related Information: Biotechnology for Biofuels; Journal ID: ISSN 1754-6834

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANAYLYTICAL CHEMISTRY; crystalline cellulose; acidothermus cellulolyticus e1 endoglucanase

Citation Formats


                    Chung, Daehwan, Young, Jenna, Cha, Minseok, Brunecky, Roman, Bomble, Yannick J., Himmel, Michael E., and Westpheling, Janet. Expression of the Acidothermus cellulolyticus E1 endoglucanase in Caldicellulosiruptor bescii enhances its ability to deconstruct crystalline cellulose.  United States: N. p., 2015. 
        Web.  doi:10.1186/s13068-015-0296-x.

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                    Chung, Daehwan, Young, Jenna, Cha, Minseok, Brunecky, Roman, Bomble, Yannick J., Himmel, Michael E., & Westpheling, Janet. Expression of the Acidothermus cellulolyticus E1 endoglucanase in Caldicellulosiruptor bescii enhances its ability to deconstruct crystalline cellulose.  United States.  https://doi.org/10.1186/s13068-015-0296-x

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                    Chung, Daehwan, Young, Jenna, Cha, Minseok, Brunecky, Roman, Bomble, Yannick J., Himmel, Michael E., and Westpheling, Janet. 2015.  
        "Expression of the Acidothermus cellulolyticus E1 endoglucanase in Caldicellulosiruptor bescii enhances its ability to deconstruct crystalline cellulose".  United States.  https://doi.org/10.1186/s13068-015-0296-x.  https://www.osti.gov/servlets/purl/1225358.

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@article{osti_1225358,

  title        = {Expression of the Acidothermus cellulolyticus E1 endoglucanase in Caldicellulosiruptor bescii enhances its ability to deconstruct crystalline cellulose},

  author       = {Chung, Daehwan and Young, Jenna and Cha, Minseok and Brunecky, Roman and Bomble, Yannick J. and Himmel, Michael E. and Westpheling, Janet},

  abstractNote = {The Caldicellulosiruptor bescii genome encodes a potent set of carbohydrate-active enzymes (CAZymes), found primarily as multi-domain enzymes that exhibit high cellulolytic and hemicellulolytic activity on and allow utilization of a broad range of substrates, including plant biomass without conventional pretreatment. CelA, the most abundant cellulase in the C. bescii secretome, uniquely combines a GH9 endoglucanase and a GH48 exoglucanase in one protein. The most effective commercial enzyme cocktails used in vitro to pretreat biomass are derived from fungal cellulases (cellobiohydrolases, endoglucanases and a β-d-glucosidases) that act synergistically to release sugars for microbial conversion. The C. bescii genome contains six GH5 domains in five different open reading frames. Four exist in multi-domain proteins and two as single catalytic domains. E1 is a GH5 endoglucanase reported to have high specific activity and simple architecture and is active at the growth temperature of C. bescii. E1 is an endo-1,4-β-glucanase linked to a family 2 carbohydrate-binding module shown to bind primarily to cellulosic substrates. As a result, we tested if the addition of this protein to the C. bescii secretome would improve its cellulolytic activity.},

  doi          = {10.1186/s13068-015-0296-x},

  url          = {https://www.osti.gov/biblio/1225358},
  journal      = {Biotechnology for Biofuels},

  issn         = {1754-6834},

  number       = 1,

  volume       = 8,

  place        = {United States},

  year         = {Thu Aug 13 00:00:00 EDT 2015},

  month        = {Thu Aug 13 00:00:00 EDT 2015}

}

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Deletion of Caldicellulosiruptor bescii CelA reveals its crucial role in the deconstruction of lignocellulosic biomass

Program Document Young, Jenna; Chung, Daehwan; Bomble, Yannick; ... - Biotechnology for Biofuels

Background: Members of the bacterial genus Caldicellulosiruptor are the most thermophilic cellulolytic organisms described to date, and have the ability to grow on lignocellulosic biomass without conventional pretreatment. Different species vary in their abilities to degrade cellulose, and the presence of CelA, a bifunctional glycoside hydrolase that contains a Family 48 and a Family 9 catalytic domain, correlates well with cellulolytic ability in members of this genus. For example, C. hydrothermalis, which does not contain a CelA homolog, or a GH48 Family or GH9 Family glycoside hydrolase, is the least cellulolytic of the Caldicellulosiruptor species so far described. C. bescii,more »« less
https://doi.org/10.1186/s13068-014-0142-6

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Characterization of the Biomass Degrading Enzyme GuxA from Acidothermus cellulolyticus

Journal Article Hengge, Neal; Mallinson, Sam; Pason, Patthra; ... - International Journal of Molecular Sciences (Online)

Microbial conversion of biomass relies on a complex combination of enzyme systems promoting synergy to overcome biomass recalcitrance. Some thermophilic bacteria have been shown to exhibit particularly high levels of cellulolytic activity, making them of particular interest for biomass conversion. These bacteria use varying combinations of CAZymes that vary in complexity from a single catalytic domain to large multi-modular and multi-functional architectures to deconstruct biomass. Since the discovery of CelA from Caldicellulosiruptor bescii which was identified as one of the most active cellulase so far identified, the search for efficient multi-modular and multi-functional CAZymes has intensified. One of these candidates,more »« less
https://doi.org/10.3390/ijms23116070
Heterologous co-expression of two β-glucanases and a cellobiose phosphorylase resulted in a significant increase in the cellulolytic activity of the Caldicellulosiruptor bescii exoproteome

Journal Article Kim, Sun-Ki; Chung, Daehwan; Himmel, Michael; ... - Journal of Industrial Microbiology and Biotechnology

The ability to deconstruct plant biomass without conventional pretreatment has made members of the genus Caldicellulosiruptor the target of investigation for the consolidated processing of plant lignocellulosic biomass to biofuels and bioproducts. To investigate the synergy of enzymes involved and to further improve the ability of C. bescii to degrade cellulose, we introduced CAZymes that act synergistically with the C. besciii exoproteome in vivo and in vitro. We recently demonstrated that the Acidothermus cellulolyticus E1 endo-1,4-β-D-glucanase (GH5) with a family 2 carbohydrate-binding module (CBM) increased the activity of C. bescii exoproteome on biomass, presumably acting in concert with CelA. Themore »« less
Cited by 8
https://doi.org/10.1007/s10295-019-02150-0
In vivo synergistic activity of a CAZyme cassette from Acidothermus cellulolyticus significantly improves the cellulolytic activity of the C. bescii exoproteome

Journal Article Kim, Sun; Chung, Daehwan; Himmel, Michael; ... - Biotechnology and Bioengineering

The use of microbial cells to convert plant biomass directly to fuels and chemicals is referred to as consolidated bioprocessing (CBP). Members of the bacterial genus, Caldicellulosiruptor (Gram-positive, anaerobic hyperthermophiles) are capable of deconstructing plant biomass without enzymatic or chemical pretreatment. This is accomplished by the production and secretion of free, multi-domain enzymes that outperform commercial enzyme cocktails on some substrates. Here, we show that the exoproteome of C. bescii may be enhanced by the heterologous expression of enzymes from Acidothermus cellulolyticus that act synergistically to improve sugar release from complex substrates; as well as improve cell growth. In thismore »« less
Cited by 10
https://doi.org/10.1002/bit.26366

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Functional Analysis of the Glucan Degradation Locus in Caldicellulosiruptor bescii Reveals Essential Roles of Component Glycoside Hydrolases in Plant Biomass Deconstruction

Journal Article Conway, Jonathan; McKinley, Bennett; Seals, Nathaniel; ... - Applied and Environmental Microbiology

We present that the ability to hydrolyze microcrystalline cellulose is an uncommon feature in the microbial world, but it can be exploited for conversion of lignocellulosic feedstocks into biobased fuels and chemicals. Understanding the physiological and biochemical mechanisms by which microorganisms deconstruct cellulosic material is key to achieving this objective. The glucan degradation locus (GDL) in the genomes of extremely thermophilic Caldicellulosiruptor species encodes polysaccharide lyases (PLs), unique cellulose binding proteins (tapirins), and putative posttranslational modifying enzymes, in addition to multidomain, multifunctional glycoside hydrolases (GHs), thereby representing an alternative paradigm for plant biomass degradation compared to fungal or cellulosomal systems.more »« less
Cited by 28
https://doi.org/10.1128/AEM.01828-17

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