Damage-free vibrational spectroscopy of biological materials in the electron microscope

Rez, Peter; Aoki, Toshihiro; March, Katia; Gur, Dvir; Krivanek, Ondrej L.; Dellby, Niklas; Lovejoy, Tracy C.; Wolf, Sharon G.; Cohen, Hagai

doi:10.1038/ncomms10945

Title: Damage-free vibrational spectroscopy of biological materials in the electron microscope

Journal Article · Thu Mar 10 00:00:00 EST 2016 · Nature Communications

DOI:https://doi.org/10.1038/ncomms10945· OSTI ID:1252902

Rez, Peter ^[1]; Aoki, Toshihiro ^[1]; March, Katia ^[2]; Gur, Dvir ^[3]; Krivanek, Ondrej L. ^[4]; Dellby, Niklas ^[5]; Lovejoy, Tracy C. ^[5];

^[3]; Cohen, Hagai ^[3]

Arizona State Univ., Tempe, AZ (United States)
Univ. Paris-Sud, Orsay (France)
Weizmann Institute of Science, Rehovot (Israel)
Arizona State Univ., Tempe, AZ (United States); Nion Co., Kirkland, WA (United States)
Nion Co., Kirkland, WA (United States)

Vibrational spectroscopy in the electron microscope would be transformative in the study of biological samples, provided that radiation damage could be prevented. However, electron beams typically create high-energy excitations that severely accelerate sample degradation. Here this major difficulty is overcome using an ‘aloof’ electron beam, positioned tens of nanometres away from the sample: high-energy excitations are suppressed, while vibrational modes of energies o1 eV can be ‘safely’ investigated. To demonstrate the potential of aloof spectroscopy, we record electron energy loss spectra from biogenic guanine crystals in their native state, resolving their characteristic C–H, N–H and C=O vibrational signatures with no observable radiation damage. Furthermore, the technique opens up the possibility of non-damaging compositional analyses of organic functional groups, including non-crystalline biological materials, at a spatial resolution of ~10nm, simultaneously combined with imaging in the electron microscope.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Rutgers Univ., New Brunswick, NJ (United States)

Sponsoring Organization:: USDOE

Contributing Organization:: Arizona State University; Universite Paris-Sud, France; Weizmann Institute of Science, Israel; Nion Co., Washington, USA

Grant/Contract Number:: SC0005132

OSTI ID:: 1252902

Journal Information:: Nature Communications, Vol. 7; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 96 works

Citation information provided by
Web of Science

References (37)

A Theoretical Study of the Electronic Spectra of Adenine and Guanine Fülscher, Markus P.; Serrano-Andrés, Luis; Roos, Björn O. Journal of the American Chemical Society, Vol. 119, Issue 26 https://doi.org/10.1021/ja964426i	journal	July 1997
Near-field probing of vibrational absorption for chemical microscopy Knoll, B.; Keilmann, F. Nature, Vol. 399, Issue 6732 https://doi.org/10.1038/20154	journal	May 1999
Vibrational-loss EELS and the avoidance of radiation damage Egerton, R. F. Ultramicroscopy, Vol. 159 https://doi.org/10.1016/j.ultramic.2015.08.003	journal	December 2015
Delocalized radiation damage in polymers Egerton, R. F.; Lazar, S.; Libera, M. Micron, Vol. 43, Issue 1 https://doi.org/10.1016/j.micron.2011.05.007	journal	January 2012
Near-Field Electron Energy Loss Spectroscopy of Nanoparticles Cohen, H.; Maniv, T.; Tenne, R. Physical Review Letters, Vol. 80, Issue 4 https://doi.org/10.1103/PhysRevLett.80.782	journal	January 1998
The Resolution Revolution Kuhlbrandt, W. Science, Vol. 343, Issue 6178 https://doi.org/10.1126/science.1251652	journal	March 2014
Cryo-EM: A Unique Tool for the Visualization of Macromolecular Complexity Nogales, Eva; Scheres, Sjors H. W. Molecular Cell, Vol. 58, Issue 4 https://doi.org/10.1016/j.molcel.2015.02.019	journal	May 2015
Vibrational spectroscopy in the electron microscope Krivanek, Ondrej L.; Lovejoy, Tracy C.; Dellby, Niklas Nature, Vol. 514, Issue 7521 https://doi.org/10.1038/nature13870	journal	October 2014
Limits to the spatial, energy and momentum resolution of electron energy-loss spectroscopy Egerton, R. F. Ultramicroscopy, Vol. 107, Issue 8 https://doi.org/10.1016/j.ultramic.2006.11.005	journal	August 2007
Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Li, Xueming; Mooney, Paul; Zheng, Shawn Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2472	journal	May 2013
Image force effects in electron microscopy Echenique, P. M.; Howie, A. Ultramicroscopy, Vol. 16, Issue 2 https://doi.org/10.1016/0304-3991(85)90082-8	journal	January 1985
The influence of fast secondary electrons on the aromatic structure of polystyrene Siangchaew, K.; Libera, M. Philosophical Magazine A, Vol. 80, Issue 4 https://doi.org/10.1080/01418610008212095	journal	May 2000
Guanine-Based Photonic Crystals in Fish Scales Form from an Amorphous Precursor Gur, Dvir; Politi, Yael; Sivan, Berta Angewandte Chemie International Edition, Vol. 52, Issue 1 https://doi.org/10.1002/anie.201205336	journal	September 2012
Examination of the secondary structure of proteins by deconvolved FTIR spectra Byler, D. Michael; Susi, Heino Biopolymers, Vol. 25, Issue 3 https://doi.org/10.1002/bip.360250307	journal	March 1986
Temperature-Sensitive, Physiologically Active Iridophores in the Lizard Urosaurus ornatus: An Ultrastructural Analysis of Color Change Morrison, Randall L.; Sherbrooke, Wade C.; Frost-Mason, Sally K. Copeia, Vol. 1996, Issue 4 https://doi.org/10.2307/1447641	journal	December 1996
Nano-FTIR Absorption Spectroscopy of Molecular Fingerprints at 20 nm Spatial Resolution Huth, Florian; Govyadinov, Alexander; Amarie, Sergiu Nano Letters, Vol. 12, Issue 8 https://doi.org/10.1021/nl301159v	journal	July 2012
Ground- and excited-state properties of DNA base molecules from plane-wave calculations using ultrasoft pseudopotentials Preuss, M.; Schmidt, W. G.; Seino, K. Journal of Computational Chemistry, Vol. 25, Issue 1 https://doi.org/10.1002/jcc.10372	journal	January 2004
Excitations at interfaces and small particles Howie, A.; Milne, R. H. Ultramicroscopy, Vol. 18, Issue 1-4 https://doi.org/10.1016/0304-3991(85)90161-5	journal	January 1985
Dielectric functions of DNA base films from near-infrared to ultra-violet Silaghi, S. D.; Friedrich, M.; Cobet, C. physica status solidi (b), Vol. 242, Issue 15 https://doi.org/10.1002/pssb.200562220	journal	December 2005
Ionization potentials and electron-donor ability of nucleic acid babes and their analogues Orlov, V. M.; Smirnov, A. N.; Varshavsky, Ya. M. Tetrahedron Letters, Vol. 17, Issue 48 https://doi.org/10.1016/0040-4039(76)80120-7	journal	November 1976
High-energy-resolution monochromator for aberration-corrected scanning transmission electron microscopy/electron energy-loss spectroscopy Krivanek, Ondrej L.; Ursin, Jonathan P.; Bacon, Neil J. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 367, Issue 1903 https://doi.org/10.1098/rsta.2009.0087	journal	September 2009
Optical excitations in electron microscopy García de Abajo, F. J. Reviews of Modern Physics, Vol. 82, Issue 1 https://doi.org/10.1103/RevModPhys.82.209	journal	February 2010
Nano-Chemical Infrared Imaging of Membrane Proteins in Lipid Bilayers Berweger, Samuel; Nguyen, Duc M.; Muller, Eric A. Journal of the American Chemical Society, Vol. 135, Issue 49 https://doi.org/10.1021/ja409815g	journal	November 2013
Radiation damage in single-particle cryo-electron microscopy: effects of dose and dose rate Karuppasamy, Manikandan; Karimi Nejadasl, Fatemeh; Vulovic, Milos Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S090904951100820X	journal	April 2011
Electron beam ionization damage processes in p-terphenyl Howie, A.; Rocca, F. J.; Valdrè, U. Philosophical Magazine B, Vol. 52, Issue 3 https://doi.org/10.1080/13642818508240634	journal	September 1985
Beam-induced motion correction for sub-megadalton cryo-EM particles Scheres, Sjors HW eLife, Vol. 3 https://doi.org/10.7554/eLife.03665	journal	August 2014
Polarizing optics in a spider eye Mueller, Kaspar P.; Labhart, Thomas Journal of Comparative Physiology A, Vol. 196, Issue 5 https://doi.org/10.1007/s00359-010-0516-6	journal	March 2010
Photonic crystals cause active colour change in chameleons Teyssier, Jérémie; Saenko, Suzanne V.; van der Marel, Dirk Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7368	journal	March 2015
Radiation damage effects at four specimen temperatures from 4 to 100K Bammes, Benjamin E.; Jakana, Joanita; Schmid, Michael F. Journal of Structural Biology, Vol. 169, Issue 3 https://doi.org/10.1016/j.jsb.2009.11.001	journal	March 2010
Valence electron excitations and plasmon oscillations in thin films, surfaces, interfaces and small particles Wang, Z. L. Micron, Vol. 27, Issue 3-4 https://doi.org/10.1016/0968-4328(96)00011-X	journal	June 1996
Mechanism of reflexion in silvery layers of fish and cephalopods Denton, Eric James; Land, M. F. Proceedings of the Royal Society of London. Series B. Biological Sciences, Vol. 178, Issue 1050, p. 43-61 https://doi.org/10.1098/rspb.1971.0051	journal	June 1971
Advances in electron microscopy: A qualitative view of instrumentation development for macromolecular imaging and tomography Schröder, Rasmus R. Archives of Biochemistry and Biophysics, Vol. 581 https://doi.org/10.1016/j.abb.2015.05.010	journal	September 2015
Electronic spectra of crystalline 9-ethylguanine and guanine hydrochloride Clark, Leigh B. Journal of the American Chemical Society, Vol. 99, Issue 12 https://doi.org/10.1021/ja00454a006	journal	June 1977
“Guanigma”: The Revised Structure of Biogenic Anhydrous Guanine Hirsch, Anna; Gur, Dvir; Polishchuk, Iryna Chemistry of Materials, Vol. 27, Issue 24 https://doi.org/10.1021/acs.chemmater.5b03549	journal	November 2015
Guanine-Based Photonic Crystals in Fish Scales Form from an Amorphous Precursor Gur, Dvir; Politi, Yael; Sivan, Berta Angewandte Chemie, Vol. 125, Issue 1 https://doi.org/10.1002/ange.201205336	journal	September 2012
Polarizing optics in a spider eye P., Mueller, K.; T., Labhart, Springer https://doi.org/10.5167/uzh-33570	text	January 2010
Optical excitations in electron microscopy de Abajo, F. J. Garcia arXiv https://doi.org/10.48550/arxiv.0903.1669	text	January 2009

Cited By (11)

Emerging Electron Microscopy Techniques for Probing Functional Interfaces in Energy Materials Zachman, Michael J.; Hachtel, Jordan A.; Idrobo, Juan Carlos Angewandte Chemie, Vol. 132, Issue 4 https://doi.org/10.1002/ange.201902993	journal	October 2019
Vibrational spectroscopy at atomic resolution with electron impact scattering Venkatraman, Kartik; Levin, Barnaby D. A.; March, Katia Nature Physics, Vol. 15, Issue 12 https://doi.org/10.1038/s41567-019-0675-5	journal	October 2019
Exploring the capabilities of monochromated electron energy loss spectroscopy in the infrared regime Hachtel, Jordan A.; Lupini, Andrew R.; Idrobo, Juan Carlos Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23805-5	journal	April 2018
The influence of surfaces and interfaces on high spatial resolution vibrational EELS from SiO2 Venkatraman, Kartik; Rez, Peter; March, Katia Microscopy, Vol. 67, Issue suppl_1 https://doi.org/10.1093/jmicro/dfy003	journal	February 2018
Identification of site-specific isotopic labels by vibrational spectroscopy in the electron microscope Hachtel, Jordan A.; Huang, Jingsong; Popovs, Ilja Science, Vol. 363, Issue 6426 https://doi.org/10.1126/science.aav5845	journal	January 2019
Evaluation of a monochromator with double cylindrical lenses for electron microscopy Ogawa, Takashi International Journal of Modern Physics A, Vol. 34, Issue 36 https://doi.org/10.1142/s0217751x19420065	journal	December 2019
Emerging Electron Microscopy Techniques for Probing Functional Interfaces in Energy Materials Zachman, Michael J.; Hachtel, Jordan A.; Idrobo, Juan Carlos Angewandte Chemie International Edition, Vol. 59, Issue 4 https://doi.org/10.1002/anie.201902993	journal	January 2020
Analytical Electron Microscopy Studies in Analytical Chemistry https://doi.org/10.1016/b978-0-444-98949-9.50011-x	book	January 1988
Analytical Electron Microscopy Freund, E.; Dexpert, H. Surface Properties and Catalysis by Non-Metals https://doi.org/10.1007/978-94-009-7160-8_8	book	January 1983
Analytical Electron Microscopy Egerton, R. F. Physical Principles of Electron Microscopy https://doi.org/10.1007/978-3-319-39877-8_6	book	July 2016
Temperature Measurement by a Nanoscale Electron Probe using Energy Gain and Loss Spectroscopy Idrobo, Juan Carlos; Lupini, Andrew R.; Feng, Tianli Microscopy and Microanalysis, Vol. 24, Issue S1 https://doi.org/10.1017/s1431927618000983	journal	August 2018

Similar Records

Mapping VIS-terahertz (=17 THz) surface plasmons sustained on native and chemically functionalized percolated gold thin films using EELS

Journal Article · Thu Mar 01 00:00:00 EST 2018 · Microscopy · OSTI ID:1252902

Abellan, Patricia; El-Khoury, Patrick Z.; Ramasse, Quentin M.

Identification of site-specific isotopic labels by vibrational spectroscopy in the electron microscope

Journal Article · Thu Jan 31 00:00:00 EST 2019 · Science · OSTI ID:1252902

Hachtel, Jordan A.; Huang, Jingsong; Popovs, Ilja; +7 more

Progress in ultrahigh energy resolution EELS

Journal Article · Tue Dec 11 00:00:00 EST 2018 · Ultramicroscopy · OSTI ID:1252902

Krivanek, Ondrej L.; Dellby, Niklas; Hachtel, Jordan A.; +9 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
physical sciences
optical physics

Title: Damage-free vibrational spectroscopy of biological materials in the electron microscope

Citation Formats

References (37)

Cited By (11)

Similar Records

Related Subjects