TY - JOUR
T1 - Electric field stimulates production of highly conductive microbial OmcZ nanowires
AU - Yalcin, Sibel Ebru
AU - O’Brien, J. Patrick
AU - Gu, Yangqi
AU - Reiss, Krystle
AU - Yi, Sophia M.
AU - Jain, Ruchi
AU - Srikanth, Vishok
AU - Dahl, Peter J.
AU - Huynh, Winston
AU - Vu, Dennis
AU - Acharya, Atanu
AU - Chaudhuri, Subhajyoti
AU - Varga, Tamas
AU - Batista, Victor S.
AU - Malvankar, Nikhil S.
N1 - Funding Information:
We thank D. Lovley (University of Massachusetts, Amherst) and K. Inoue (University of Miyazaki) for providing strains and OmcZ antibody as well as E. Yan, E. Martz, F. Samatey, C. Salgueiro, C. Shipps and Y. Xiong for helpful discussions. We also thank C. Leang for providing the protocol for immunogold labeling, T. Gokus from Neaspec for help with nanoscale IR imaging and M. Shahid Mansuri, J. Kanyo and T. Lam for help with mass-spectrometry analysis. A portion of the research was performed using Environmental Molecular Sciences Laboratory (EMSL, Ringgold ID 130367), a Department of Energy (DOE) Office of Science User Facility sponsored by the Office of Biological and Environmental Research. S.E.Y. thanks M. Raschke, J. Atkin and S. Lea for help with building the IR s-SNOM setup and C. Smallwood for help with bacteriorhodopsin sample preparation. We thank T. Walsh from Asylum Research for help with stiffness measurements. At Yale, we thank W. Gray from C. Jacobs-Wagner’s laboratory for help with fluorescence microscopy and Z. Wu from H. Wang’s laboratory for help with Raman studies. Computational work was supported by the Air Force Office of Scientific Research Grant FA9550-17-0198 (V.S.B.) and high-performance computing time from the National Energy Research Scientific Computing Center and from the high-performance computing facilities at Yale as well as supercomputer time from the Extreme Science and Engineering Discovery Environment under grant no. TG-CHE170024 (A.A.). Anton 2 computer time was provided by the Pittsburgh Supercomputing Center (PSC) through Grant R01GM116961 from the National Institutes of Health (NIH). The Anton 2 machine at PSC was generously made available by D.E. Shaw Research. This research was supported by the Career Award at the Scientific Interfaces from Burroughs Welcome Fund (N.S.M.), the NIH Director’s New Innovator award no. 1DP2AI138259-01 (N.S.M.), the National Science Foundation (NSF) CAREER award no. 1749662 (N.S.M.). Research was sponsored by the Defense Advanced Research Project Agency Army Research Office and was accomplished under Cooperative Agreement Number W911NF-18-2-0100 (N.S.M. and V.S.B). This research was supported by NSF Graduate Research Fellowship awards 2017224445 (J.P.O.). Research in the laboratory is also supported by the Charles H. Hood Foundation Child Health Research Award (N.S.M.) and The Hartwell Foundation Individual Biomedical Research Award (N.S.M.).
Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature America, Inc.
PY - 2020/10/1
Y1 - 2020/10/1
N2 - Multifunctional living materials are attractive due to their powerful ability to self-repair and replicate. However, most natural materials lack electronic functionality. Here we show that an electric field, applied to electricity-producing Geobacter sulfurreducens biofilms, stimulates production of cytochrome OmcZ nanowires with 1,000-fold higher conductivity (30 S cm−1) and threefold higher stiffness (1.5 GPa) than the cytochrome OmcS nanowires that are important in natural environments. Using chemical imaging-based multimodal nanospectroscopy, we correlate protein structure with function and observe pH-induced conformational switching to β-sheets in individual nanowires, which increases their stiffness and conductivity by 100-fold due to enhanced π-stacking of heme groups; this was further confirmed by computational modeling and bulk spectroscopic studies. These nanowires can transduce mechanical and chemical stimuli into electrical signals to perform sensing, synthesis and energy production. These findings of biologically produced, highly conductive protein nanowires may help to guide the development of seamless, bidirectional interfaces between biological and electronic systems. [Figure not available: see fulltext.].
AB - Multifunctional living materials are attractive due to their powerful ability to self-repair and replicate. However, most natural materials lack electronic functionality. Here we show that an electric field, applied to electricity-producing Geobacter sulfurreducens biofilms, stimulates production of cytochrome OmcZ nanowires with 1,000-fold higher conductivity (30 S cm−1) and threefold higher stiffness (1.5 GPa) than the cytochrome OmcS nanowires that are important in natural environments. Using chemical imaging-based multimodal nanospectroscopy, we correlate protein structure with function and observe pH-induced conformational switching to β-sheets in individual nanowires, which increases their stiffness and conductivity by 100-fold due to enhanced π-stacking of heme groups; this was further confirmed by computational modeling and bulk spectroscopic studies. These nanowires can transduce mechanical and chemical stimuli into electrical signals to perform sensing, synthesis and energy production. These findings of biologically produced, highly conductive protein nanowires may help to guide the development of seamless, bidirectional interfaces between biological and electronic systems. [Figure not available: see fulltext.].
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U2 - 10.1038/s41589-020-0623-9
DO - 10.1038/s41589-020-0623-9
M3 - Article
C2 - 32807967
AN - SCOPUS:85089541066
SN - 1552-4450
VL - 16
SP - 1136
EP - 1142
JO - Nature Chemical Biology
JF - Nature Chemical Biology
IS - 10
ER -