Acoustic force spectroscopy reveals subtle differences in cellulose unbinding behavior of carbohydrate-binding modules

Hackl, Markus; Contrada, Edward V.; Ash, Jonathan E.; Kulkarni, Atharv; Yoon, Jinho; Cho, Hyeon-Yeol; Lee, Ki-Bum; Yarbrough, John M.; López, Cesar A.; Gnanakaran, Sandrasegaram; Chundawat, Shishir P. S.

doi:10.1073/pnas.2117467119

Title: Acoustic force spectroscopy reveals subtle differences in cellulose unbinding behavior of carbohydrate-binding modules

Journal Article · Mon Oct 10 00:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2117467119· OSTI ID:1891584

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^[1]; Kulkarni, Atharv ^[1]; Yoon, Jinho ^[2];

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^[3]; López, Cesar A. ^[4];

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Department of Chemical and Biochemical Engineering, Rutgers, The State University of New Jersey, Piscataway, NJ 08854
Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, Piscataway, NJ 08854
Biosciences Center, National Renewable Energy Laboratory, Golden, CO 80401
Theoretical Division, Los Alamos National Laboratory, Los Alamos, NM 87545

Protein adsorption to solid carbohydrate interfaces is critical to many biological processes, particularly in biomass deconstruction. To engineer more-efficient enzymes for biomass deconstruction into sugars, it is necessary to characterize the complex protein–carbohydrate interfacial interactions. A carbohydrate-binding module (CBM) is often associated with microbial surface-tethered cellulosomes or secreted cellulase enzymes to enhance substrate accessibility. However, it is not well known how CBMs recognize, bind, and dissociate from polysaccharides to facilitate efficient cellulolytic activity, due to the lack of mechanistic understanding and a suitable toolkit to study CBM–substrate interactions. Our work outlines a general approach to study the unbinding behavior of CBMs from polysaccharide surfaces using a highly multiplexed single-molecule force spectroscopy assay. Here, we apply acoustic force spectroscopy (AFS) to probe a Clostridium thermocellum cellulosomal scaffoldin protein (CBM3a) and measure its dissociation from nanocellulose surfaces at physiologically relevant, low force loading rates. An automated microfluidic setup and method for uniform deposition of insoluble polysaccharides on the AFS chip surfaces are demonstrated. The rupture forces of wild-type CBM3a, and its Y67A mutant, unbinding from nanocellulose surfaces suggests distinct multimodal CBM binding conformations, with structural mechanisms further explored using molecular dynamics simulations. Further, applying classical dynamic force spectroscopy theory, the single-molecule unbinding rate at zero force is extrapolated and found to agree with bulk equilibrium unbinding rates estimated independently using quartz crystal microbalance with dissipation monitoring. However, our results also highlight critical limitations of applying classical theory to explain the highly multivalent binding interactions for cellulose–CBM bond rupture forces exceeding 15 pN.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE); USDOE Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF); New Jersey Commission on Spinal Cord; National Institutes of Health (NIH)

Grant/Contract Number:: LANL LDRD ER (XWX2; 28598; AC36-08GO28308; CBET-1846797; CBET-1803517; CSCR17IRG010; CSCR16ERG019; 1R01DC016612; 3R01DC016612-01S1; 5R01DC016612-02S1; 89233218CNA000001

OSTI ID:: 1891584

Alternate ID(s):: OSTI ID: 1900023; OSTI ID: 2008278

Report Number(s):: NREL/JA-2700-84628; LA-UR-22-23938; e2117467119

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 119 Journal Issue: 42; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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09 BIOMASS FUELS
acoustic force spectroscopy
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carbohydrate-binding module
nanocellulose
single-molecule force spectroscopy

Title: Acoustic force spectroscopy reveals subtle differences in cellulose unbinding behavior of carbohydrate-binding modules

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