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Enzymology and Protein Engineering

Two Distinct α-l-Arabinofuranosidases in Caldicellulosiruptor Species Drive Degradation of Arabinose-Based Polysaccharides

Mohammad Abu Saleh, Wen-Jie Han, Ming Lu, Bing Wang, Huayue Li, Robert M. Kelly, Fu-Li Li
Harold L. Drake, Editor
Mohammad Abu Saleh
aShandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuel, Qingdao Engineering Laboratory of Single Cell Oil, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, and University of Chinese Academy of Sciences, Beijing, People's Republic of China
bDepartment of Genetic Engineering and Biotechnology, University of Rajshahi, Rajshahi, Bangladesh
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Wen-Jie Han
aShandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuel, Qingdao Engineering Laboratory of Single Cell Oil, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, and University of Chinese Academy of Sciences, Beijing, People's Republic of China
cCollege of Environmental Science and Engineering, Qingdao University, Qingdao, China
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Ming Lu
aShandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuel, Qingdao Engineering Laboratory of Single Cell Oil, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, and University of Chinese Academy of Sciences, Beijing, People's Republic of China
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Bing Wang
aShandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuel, Qingdao Engineering Laboratory of Single Cell Oil, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, and University of Chinese Academy of Sciences, Beijing, People's Republic of China
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Huayue Li
dSchool of Medicine and Pharmacy, Ocean University of China, Qingdao, China
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Robert M. Kelly
eDepartment of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, North Carolina, USA
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Fu-Li Li
aShandong Provincial Key Laboratory of Energy Genetics, Key Laboratory of Biofuel, Qingdao Engineering Laboratory of Single Cell Oil, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, and University of Chinese Academy of Sciences, Beijing, People's Republic of China
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Harold L. Drake
University of Bayreuth
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DOI: 10.1128/AEM.00574-17
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ABSTRACT

Species in the extremely thermophilic genus Caldicellulosiruptor can degrade unpretreated plant biomass through the action of multimodular glycoside hydrolases. To date, most focus with these bacteria has been on hydrolysis of glucans and xylans, while the biodegradation mechanism for arabinose-based polysaccharides remains unclear. Here, putative α-l-arabinofuranosidases (AbFs) were identified in Caldicellulosiruptor species by homology to less-thermophilic versions of these enzymes. From this screen, an extracellular XynF was determined to be a key factor in hydrolyzing α-1,2-, α-1,3-, and α-1,5-l-arabinofuranosyl residues of arabinose-based polysaccharides. Combined with a GH11 xylanase (XynA), XynF increased arabinoxylan hydrolysis more than 6-fold compared to the level seen with XynA alone, likely the result of XynF removing arabinofuranosyl side chains to generate linear xylans that were readily degraded. A second AbF, the intracellular AbF51, preferentially cleaved the α-1,5-l-arabinofuranosyl glycoside bonds within sugar beet arabinan. β-Xylosidases, such as GH39 Xyl39B, facilitated the hydrolysis of arabinofuranosyl residues at the nonreducing terminus of the arabinose-branched xylo-oligosaccharides by AbF51. These results demonstrate the separate but complementary contributions of extracellular XynF and cytosolic AbF51 in processing the bioconversion of arabinose-containing oligosaccharides to fermentable monosaccharides.

IMPORTANCE Degradation of hemicellulose, due to its complex chemical structure, presents a major challenge during bioconversion of lignocellulosic biomass to biobased fuels and chemicals. Degradation of arabinose-containing polysaccharides, in particular, can be a key bottleneck in this process. Among Caldicellulosiruptor species, the multimodular arabinofuranosidase XynF is present in only selected members of this genus. This enzyme exhibited high hydrolysis activity, broad specificity, and strong synergism with other hemicellulases acting on arabino-polysaccharides. An intracellular arabinofuranosidase, AbF51, occurs in all Caldicellulosiruptor species and, in conjunction with xylosidases, processes the bioconversion of arabinose-branched oligosaccharides to fermentable monosaccharides. Taken together, the data suggest that plant biomass degradation in Caldicellulosiruptor species involves extracellular XynF that acts synergistically with other hemicellulases to digest arabino-polysaccharides that are subsequently transported and degraded further by intracellular AbF51 to produce short-chain arabino sugars.

FOOTNOTES

    • Received 9 March 2017.
    • Accepted 17 April 2017.
    • Accepted manuscript posted online 21 April 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.00574-17 .

  • Copyright © 2017 American Society for Microbiology.

All Rights Reserved .

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Two Distinct α-l-Arabinofuranosidases in Caldicellulosiruptor Species Drive Degradation of Arabinose-Based Polysaccharides
Mohammad Abu Saleh, Wen-Jie Han, Ming Lu, Bing Wang, Huayue Li, Robert M. Kelly, Fu-Li Li
Applied and Environmental Microbiology Jun 2017, 83 (13) e00574-17; DOI: 10.1128/AEM.00574-17

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Two Distinct α-l-Arabinofuranosidases in Caldicellulosiruptor Species Drive Degradation of Arabinose-Based Polysaccharides
Mohammad Abu Saleh, Wen-Jie Han, Ming Lu, Bing Wang, Huayue Li, Robert M. Kelly, Fu-Li Li
Applied and Environmental Microbiology Jun 2017, 83 (13) e00574-17; DOI: 10.1128/AEM.00574-17
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KEYWORDS

Arabinose
Bacterial Proteins
Firmicutes
glycoside hydrolases
polysaccharides
Arabinofuranosidase
bioenergy
glycoside hydrolase
hyperthermophiles
synergism

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