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Research Article

Comparative Community Proteomics Demonstrates the Unexpected Importance of Actinobacterial Glycoside Hydrolase Family 12 Protein for Crystalline Cellulose Hydrolysis

Jennifer Hiras, Yu-Wei Wu, Kai Deng, Carrie D. Nicora, Joshua T. Aldrich, Dario Frey, Sebastian Kolinko, Errol W. Robinson, Jon M. Jacobs, Paul D. Adams, Trent R. Northen, Blake A. Simmons, Steven W. Singer
Sang Yup Lee, Editor
Jennifer Hiras
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Yu-Wei Wu
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Kai Deng
Joint BioEnergy Institute, Emeryville, California, USABiological and Materials Science Center, Sandia National Laboratories, Livermore, California, USA
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Carrie D. Nicora
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Joshua T. Aldrich
Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA
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Dario Frey
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USAFaculty of Biotechnology, University of Applied Sciences Mannheim, Mannheim, Germany
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Sebastian Kolinko
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Errol W. Robinson
Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, Washington, USA
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Jon M. Jacobs
Biological Sciences Division, Pacific Northwest National Laboratory, Richland, Washington, USA
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Paul D. Adams
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Trent R. Northen
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Blake A. Simmons
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Steven W. Singer
Joint BioEnergy Institute, Emeryville, California, USABiosciences Directorate, Lawrence Berkeley National Laboratory, Berkeley, California, USA
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Sang Yup Lee
Korea Advanced Institute of Science and Technology
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DOI: 10.1128/mBio.01106-16
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ABSTRACT

Glycoside hydrolases (GHs) are key enzymes in the depolymerization of plant-derived cellulose, a process central to the global carbon cycle and the conversion of plant biomass to fuels and chemicals. A limited number of GH families hydrolyze crystalline cellulose, often by a processive mechanism along the cellulose chain. During cultivation of thermophilic cellulolytic microbial communities, substantial differences were observed in the crystalline cellulose saccharification activities of supernatants recovered from divergent lineages. Comparative community proteomics identified a set of cellulases from a population closely related to actinobacterium Thermobispora bispora that were highly abundant in the most active consortium. Among the cellulases from T. bispora, the abundance of a GH family 12 (GH12) protein correlated most closely with the changes in crystalline cellulose hydrolysis activity. This result was surprising since GH12 proteins have been predominantly characterized as enzymes active on soluble polysaccharide substrates. Heterologous expression and biochemical characterization of the suite of T. bispora hydrolytic cellulases confirmed that the GH12 protein possessed the highest activity on multiple crystalline cellulose substrates and demonstrated that it hydrolyzes cellulose chains by a predominantly random mechanism. This work suggests that the role of GH12 proteins in crystalline cellulose hydrolysis by cellulolytic microbes should be reconsidered.

IMPORTANCE Cellulose is the most abundant organic polymer on earth, and its enzymatic hydrolysis is a key reaction in the global carbon cycle and the conversion of plant biomass to biofuels. The glycoside hydrolases that depolymerize crystalline cellulose have been primarily characterized from isolates. In this study, we demonstrate that adapting microbial consortia from compost to grow on crystalline cellulose generated communities whose soluble enzymes exhibit differential abilities to hydrolyze crystalline cellulose. Comparative proteomics of these communities identified a protein of glycoside hydrolase family 12 (GH12), a family of proteins previously observed to primarily hydrolyze soluble substrates, as a candidate that accounted for some of the differences in hydrolytic activities. Heterologous expression confirmed that the GH12 protein identified by proteomics was active on crystalline cellulose and hydrolyzed cellulose by a random mechanism, in contrast to most cellulases that act on the crystalline polymer in a processive mechanism.

  • Copyright © 2016 Hiras et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Comparative Community Proteomics Demonstrates the Unexpected Importance of Actinobacterial Glycoside Hydrolase Family 12 Protein for Crystalline Cellulose Hydrolysis
Jennifer Hiras, Yu-Wei Wu, Kai Deng, Carrie D. Nicora, Joshua T. Aldrich, Dario Frey, Sebastian Kolinko, Errol W. Robinson, Jon M. Jacobs, Paul D. Adams, Trent R. Northen, Blake A. Simmons, Steven W. Singer
mBio Aug 2016, 7 (4) e01106-16; DOI: 10.1128/mBio.01106-16

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Comparative Community Proteomics Demonstrates the Unexpected Importance of Actinobacterial Glycoside Hydrolase Family 12 Protein for Crystalline Cellulose Hydrolysis
Jennifer Hiras, Yu-Wei Wu, Kai Deng, Carrie D. Nicora, Joshua T. Aldrich, Dario Frey, Sebastian Kolinko, Errol W. Robinson, Jon M. Jacobs, Paul D. Adams, Trent R. Northen, Blake A. Simmons, Steven W. Singer
mBio Aug 2016, 7 (4) e01106-16; DOI: 10.1128/mBio.01106-16
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