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Title: Discrete and Structurally Unique Proteins (T$$\bar{a}$$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose

Abstract

A variety of catalytic and noncatalytic protein domains are deployed by select microorganisms to deconstruct lignocellulose. These extracellular proteins are used to attach to, modify, and hydrolyze the complex polysaccharides present in plant cell walls. Cellulolytic enzymes, often containing carbohydrate-binding modules, are key to this process; however, these enzymes are not solely responsible for attachment. Few mechanisms of attachment have been discovered among bacteria that do not form large polypeptide structures, called cellulosomes, to deconstruct biomass. In this study, bioinformatics and proteomics analyses identified unique, discrete, hypothetical proteins (“t$$\bar{a}$$pirins,” origin from M$$\bar{a}$$ori: to join), not directly associated with cellulases, that mediate attachment to cellulose by species in the noncellulosomal, extremely thermophilic bacterial genus Caldicellulosiruptor. Two t$$\bar{a}$$pirin genes are located directly downstream of a type IV pilus operon in strongly cellulolytic members of the genus, whereas homologs are absent from the weakly cellulolytic Caldicellulosiruptor species. Based on their amino acid sequence, t$$\bar{a}$$pirins are specific to these extreme thermophiles. T$$\bar{a}$$pirins are also unusual in that they share no detectable protein domain signatures with known polysaccharide-binding proteins. Adsorption isotherm and trans vivo analyses demonstrated the carbohydrate-binding module-like affinity of the t$$\bar{a}$$pirins for cellulose. Crystallization of a cellulose-binding truncation from one t$$\bar{a}$$pirin indicated that these proteins form a long β-helix core with a shielded hydrophobic face. In addition, they are structurally unique and define a new class of polysaccharide adhesins. Strongly cellulolytic Caldicellulosiruptor species employ t$$\bar{a}$$pirins to complement substrate-binding proteins from the ATP-binding cassette transporters and multidomain extracellular and S-layer-associated glycoside hydrolases to process the carbohydrate content of lignocellulose.

Authors:
 [1];  [2];  [1];  [1];  [1];  [3];  [3];  [2];  [2];  [1]
+ Show Author Affiliations
  1. North Carolina State Univ., Raleigh, NC (United States). Dept. of Chemical and Biomolecular Engineering
  2. National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1286760
Alternate Identifier(s):
OSTI ID: 1220749
Report Number(s):
NREL/JA-2700-64273
Journal ID: ISSN 0021-9258; KP1601050; ERKP695
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 290; Journal Issue: 17; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; adhesin; bacteria; biodegradation; cellulose; extreme thermophile; protein structure; caldicellulosiruptor; cellulose-binding protein

Citation Formats

Blumer-Schuette, Sara E., Alahuhta, Markus, Conway, Jonathan M., Lee, Laura L., Zurawski, Jeffrey V., Giannone, Richard J., Hettich, Robert L., Lunin, Vladimir V., Himmel, Michael E., and Kelly, Robert M. Discrete and Structurally Unique Proteins (T$\bar{a}$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose. United States: N. p., 2015. Web. doi:10.1074/jbc.M115.641480.
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Blumer-Schuette, Sara E., Alahuhta, Markus, Conway, Jonathan M., Lee, Laura L., Zurawski, Jeffrey V., Giannone, Richard J., Hettich, Robert L., Lunin, Vladimir V., Himmel, Michael E., & Kelly, Robert M. Discrete and Structurally Unique Proteins (T$\bar{a}$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose. United States. https://doi.org/10.1074/jbc.M115.641480
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Blumer-Schuette, Sara E., Alahuhta, Markus, Conway, Jonathan M., Lee, Laura L., Zurawski, Jeffrey V., Giannone, Richard J., Hettich, Robert L., Lunin, Vladimir V., Himmel, Michael E., and Kelly, Robert M. Thu . "Discrete and Structurally Unique Proteins (T$\bar{a}$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose". United States. https://doi.org/10.1074/jbc.M115.641480. https://www.osti.gov/servlets/purl/1286760.
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@article{osti_1286760,
title = {Discrete and Structurally Unique Proteins (T$\bar{a}$pirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose},
author = {Blumer-Schuette, Sara E. and Alahuhta, Markus and Conway, Jonathan M. and Lee, Laura L. and Zurawski, Jeffrey V. and Giannone, Richard J. and Hettich, Robert L. and Lunin, Vladimir V. and Himmel, Michael E. and Kelly, Robert M.},
abstractNote = {A variety of catalytic and noncatalytic protein domains are deployed by select microorganisms to deconstruct lignocellulose. These extracellular proteins are used to attach to, modify, and hydrolyze the complex polysaccharides present in plant cell walls. Cellulolytic enzymes, often containing carbohydrate-binding modules, are key to this process; however, these enzymes are not solely responsible for attachment. Few mechanisms of attachment have been discovered among bacteria that do not form large polypeptide structures, called cellulosomes, to deconstruct biomass. In this study, bioinformatics and proteomics analyses identified unique, discrete, hypothetical proteins (“t$\bar{a}$pirins,” origin from M$\bar{a}$ori: to join), not directly associated with cellulases, that mediate attachment to cellulose by species in the noncellulosomal, extremely thermophilic bacterial genus Caldicellulosiruptor. Two t$\bar{a}$pirin genes are located directly downstream of a type IV pilus operon in strongly cellulolytic members of the genus, whereas homologs are absent from the weakly cellulolytic Caldicellulosiruptor species. Based on their amino acid sequence, t$\bar{a}$pirins are specific to these extreme thermophiles. T$\bar{a}$pirins are also unusual in that they share no detectable protein domain signatures with known polysaccharide-binding proteins. Adsorption isotherm and trans vivo analyses demonstrated the carbohydrate-binding module-like affinity of the t$\bar{a}$pirins for cellulose. Crystallization of a cellulose-binding truncation from one t$\bar{a}$pirin indicated that these proteins form a long β-helix core with a shielded hydrophobic face. In addition, they are structurally unique and define a new class of polysaccharide adhesins. Strongly cellulolytic Caldicellulosiruptor species employ t$\bar{a}$pirins to complement substrate-binding proteins from the ATP-binding cassette transporters and multidomain extracellular and S-layer-associated glycoside hydrolases to process the carbohydrate content of lignocellulose.},
doi = {10.1074/jbc.M115.641480},
journal = {Journal of Biological Chemistry},
number = 17,
volume = 290,
place = {United States},
year = {Thu Feb 26 00:00:00 EST 2015},
month = {Thu Feb 26 00:00:00 EST 2015}
}
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