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

Blumer-Schuette, S. E.; Alahuhta, M.; Conway, J. M.; Lee, L. L.; Zurawski, J. V.; Giannone, Richard J.; Hettich, R. L.; Lunin, V. V.; HImmel, M. E.; Kelly, R. M.

doi:10.1074/jbc.M115.641480

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

Journal Article · Fri Apr 24 00:00:00 EDT 2015 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.M115.641480· OSTI ID:1220749

Blumer-Schuette, S. E. ^[1]; Alahuhta, M. ^[2]; Conway, J. M. ^[1]; Lee, L. L. ^[1]; Zurawski, J. V. ^[1]; Giannone, Richard J. ^[3]; Hettich, R. L. ^[3]; Lunin, V. V. ^[2]; HImmel, M. E. ^[2]; Kelly, R. M. ^[1]

North Carolina State Univ., Raleigh, NC (United States). Dept. of Chemical and Biomolecular Engineering
National Renewable Energy Lab. (NREL), Golden, CO (United States). Biosciences Center
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division

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.

View Accepted Manuscript (DOE)

Research Organization:: NREL (National Renewable Energy Laboratory (NREL), Golden, CO (United States)); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)

Sponsoring Organization:: USDOE Office of Science (SC); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1220749

Alternate ID(s):: OSTI ID: 1286760

Report Number(s):: NREL/JA--2700-64273

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 17 Vol. 290; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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