Electric field stimulates production of highly conductive microbial OmcZ nanowires

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...

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Published inNature chemical biology Vol. 16; no. 10; pp. 1136 - 1142
Main Authors Yalcin, Sibel Ebru, O'Brien, J Patrick, Gu, Yangqi, Reiss, Krystle, Yi, Sophia M, Jain, Ruchi, Srikanth, Vishok, Dahl, Peter J, Huynh, Winston, Vu, Dennis, Acharya, Atanu, Chaudhuri, Subhajyoti, Varga, Tamas, Batista, Victor S, Malvankar, Nikhil S
Format Journal Article
LanguageEnglish
Published United States Nature Publishing Group 01.10.2020
Subjects
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
BASIC BIOLOGICAL SCIENCES
Biochemistry
Biofilms
biological techniques
biophysics
chemical biology
Chemical stimuli
computational biology and bioinformatics
Computer applications
Conductivity
Cytochrome
Cytochromes
Electric Conductivity
Electric fields
Electric Stimulation
Electrical resistivity
Electronic systems
Electrophysiological Phenomena
Geobacter - physiology
Geobacter sulfurreducens
Heme
INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Interfaces
Microorganisms
Nanotechnology
Nanowires
Nanowires - chemistry
pH effects
Protein structure
Proteins
Stacking
Stiffness
Structure-function relationships
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Summary: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 ) 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.
Bibliography:Defense Advanced Research Project Agency (DARPA)
USDOE Office of Science (SC)
PNNL-SA-132842
National Institutes of Health (NIH)
AC05-76RL01830; 1DP2AI138259-01; 1749662; W911NF-18-2-0100; 2017224445; R01GM116961
National Science Foundation (NSF)
US Air Force Office of Scientific Research (AFOSR)
Author Contributions S.E.Y. and N.S.M. conceived and designed the study. S.E.Y. built the quantum cascade laser-coupled IR s-SNOM detection interferometer, prepared samples, performed AFM, IR s-SNOM measurements, imaged immunogold labelled nanowires with AFM along with imaging and analysis of reduction in nanowire diameter. J.P.O. grew biofilms in microbial fuel cell and analysed protein content with R.J. K.R. built the OmcZ model and performed simulations, with help from P.J.D., under the guidance of V.S.B. J.P.O. and W.H. purified nanowire from bacteria, performed CD experiments, and conducted analysis. J.P.O. performed FTIR and fluorescence emission spectroscopy and analysed data with S.E.Y. W.H. and S.E.Y. performed principal component analysis on the IR s-SNOM data. V.S. and Y.G. imaged immunogold labelled nanowires with TEM. Y.G. also carried out CP-AFM measurements and analysed data with P.J.D. Y.G. and S.E.Y performed and analysed nanowire stiffness measurements. S.M.Y. carried out mass spectroscopy as well as Raman spectroscopy and analysed Raman data with S.E.Y. Electrode fabrication using electron beam lithography was carried out by D. V. and Y. G. S. E. Y. and T. V. performed XRD measurements and analysed data with Y.G. A.A. and S.C. performed initial molecular dynamics simulations under the guidance of V.S.B. A.A. constructed the models, coded the analysis scripts, and performed the analysis of molecular dynamics data. N.S.M. supervised the project. S.E.Y. and N.S.M. cowrote the manuscript with input from all authors.
ISSN:1552-4450
1552-4469
DOI:10.1038/s41589-020-0623-9