skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Off-axis electron holography of bacterial cells and magnetic nanoparticles in liquid

Abstract

Here, the mapping of electrostatic potentials and magnetic fields in liquids using electron holography has been considered to be unrealistic. Here, we show that hydrated cells of Magnetospirillum magneticum strain AMB-1 and assemblies of magnetic nanoparticles can be studied using off-axis electron holography in a fluid cell specimen holder within the transmission electron microscope. Considering that the holographic object and reference wave both pass through liquid, the recorded electron holograms show sufficient interference fringe contrast to permit reconstruction of the phase shift of the electron wave and mapping of the magnetic induction from bacterial magnetite nanocrystals. We assess the challenges of performing in situ magnetization reversal experiments using a fluid cell specimen holder, discuss approaches for improving spatial resolution and specimen stability, and outline future perspectives for studying scientific phenomena, ranging from interparticle interactions in liquids and electrical double layers at solid–liquid interfaces to biomineralization and the mapping of electrostatic potentials associated with protein aggregation and folding.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [3]
  1. Ames Lab., Ames, IA (United States)
  2. Imperial College London, London (United Kingdom)
  3. Forschungszentrum Julich, Julich (Germany)
Publication Date:
Research Org.:
Ames Lab., Ames, IA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1406562
Report Number(s):
IS-J-9452
Journal ID: ISSN 1742-5689; TRN: US1703042
Grant/Contract Number:  
AC02-07CH11358; (FP7/2007-2013); 320832
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the Royal Society Interface
Additional Journal Information:
Journal Volume: 14; Journal Issue: 135; Journal ID: ISSN 1742-5689
Publisher:
The Royal Society
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; 75 CONDENSED MATTER PHYSICS, SUPERCONDUCTIVITY AND SUPERFLUIDITY

Citation Formats

Prozorov, Tanya, Almeida, Trevor P., Kovacs, Andras, and Dunin-Borkowski, Rafal E. Off-axis electron holography of bacterial cells and magnetic nanoparticles in liquid. United States: N. p., 2017. Web. doi:10.1098/rsif.2017.0464.
Prozorov, Tanya, Almeida, Trevor P., Kovacs, Andras, & Dunin-Borkowski, Rafal E. Off-axis electron holography of bacterial cells and magnetic nanoparticles in liquid. United States. doi:10.1098/rsif.2017.0464.
Prozorov, Tanya, Almeida, Trevor P., Kovacs, Andras, and Dunin-Borkowski, Rafal E. Mon . "Off-axis electron holography of bacterial cells and magnetic nanoparticles in liquid". United States. doi:10.1098/rsif.2017.0464. https://www.osti.gov/servlets/purl/1406562.
@article{osti_1406562,
title = {Off-axis electron holography of bacterial cells and magnetic nanoparticles in liquid},
author = {Prozorov, Tanya and Almeida, Trevor P. and Kovacs, Andras and Dunin-Borkowski, Rafal E.},
abstractNote = {Here, the mapping of electrostatic potentials and magnetic fields in liquids using electron holography has been considered to be unrealistic. Here, we show that hydrated cells of Magnetospirillum magneticum strain AMB-1 and assemblies of magnetic nanoparticles can be studied using off-axis electron holography in a fluid cell specimen holder within the transmission electron microscope. Considering that the holographic object and reference wave both pass through liquid, the recorded electron holograms show sufficient interference fringe contrast to permit reconstruction of the phase shift of the electron wave and mapping of the magnetic induction from bacterial magnetite nanocrystals. We assess the challenges of performing in situ magnetization reversal experiments using a fluid cell specimen holder, discuss approaches for improving spatial resolution and specimen stability, and outline future perspectives for studying scientific phenomena, ranging from interparticle interactions in liquids and electrical double layers at solid–liquid interfaces to biomineralization and the mapping of electrostatic potentials associated with protein aggregation and folding.},
doi = {10.1098/rsif.2017.0464},
journal = {Journal of the Royal Society Interface},
number = 135,
volume = 14,
place = {United States},
year = {2017},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Imaging Specific Protein Labels on Eukaryotic Cells in Liquid with Scanning Transmission Electron Microscopy
journal, August 2011


Electron microscopy of specimens in liquid
journal, October 2011

  • de Jonge, Niels; Ross, Frances M.
  • Nature Nanotechnology, Vol. 6, Issue 11, p. 695-704
  • DOI: 10.1038/nnano.2011.161

Magnetosome vesicles are present before magnetite formation, and MamA is required for their activation
journal, March 2004

  • Komeili, A.; Vali, H.; Beveridge, T. J.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 11
  • DOI: 10.1073/pnas.0400391101

Electron holography of non-stained bacterial surface layer proteins
journal, May 2004

  • Simon, P.; Lichte, H.; Wahl, R.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1663, Issue 1-2
  • DOI: 10.1016/j.bbamem.2004.03.005

The extraordinary dielectric properties of biological materials and the action of enzymes.
journal, November 1975


Understanding the Surface Potential of Water
journal, April 2011

  • Kathmann, Shawn M.; Kuo, I-Feng William; Mundy, Christopher J.
  • The Journal of Physical Chemistry B, Vol. 115, Issue 15
  • DOI: 10.1021/jp1116036

Electron tomography and holography in materials science
journal, April 2009

  • Midgley, Paul A.; Dunin-Borkowski, Rafal E.
  • Nature Materials, Vol. 8, Issue 4
  • DOI: 10.1038/nmat2406

X-rays Reveal the Internal Structure of Keratin Bundles in Whole Cells
journal, February 2016

  • Hémonnot, Clément Y. J.; Reinhardt, Juliane; Saldanha, Oliva
  • ACS Nano, Vol. 10, Issue 3
  • DOI: 10.1021/acsnano.5b07871

Bubble and Pattern Formation in Liquid Induced by an Electron Beam
journal, December 2013

  • Grogan, Joseph M.; Schneider, Nicholas M.; Ross, Frances M.
  • Nano Letters, Vol. 14, Issue 1
  • DOI: 10.1021/nl404169a

Magnetite formation by a magnetic bacterium capable of growing aerobically
journal, August 1991

  • Matsunaga, Tadashi; Sakaguchi, Toshifumi; Tadakoro, Fumihiko
  • Applied Microbiology and Biotechnology, Vol. 35, Issue 5
  • DOI: 10.1007/BF00169632

Beamstop-based low-background ptychography to image weakly scattering objects
journal, February 2017


Magnetite from magnetotactic bacteria; size distributions and twinning
journal, December 1998

  • Devouard, Bertrand; Posfai, Mihaly; Hua, Xin
  • American Mineralogist, Vol. 83, Issue 11-12 Part 2
  • DOI: 10.2138/am-1998-11-1228

Off-axis electron holography of exchange-biased CoFe/FeMn patterned nanostructures
journal, September 2001

  • Dunin-Borkowski, R. E.; McCartney, M. R.; Kardynal, B.
  • Journal of Applied Physics, Vol. 90, Issue 6
  • DOI: 10.1063/1.1390493

An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria
journal, November 2005

  • Scheffel, André; Gruska, Manuela; Faivre, Damien
  • Nature, Vol. 440, Issue 7080
  • DOI: 10.1038/nature04382

Bulge testing of copper and niobium tubes for hydroformed RF cavities
journal, January 2016


Nucleation of Iron Oxide Nanoparticles Mediated by Mms6 Protein in Situ
journal, August 2014

  • Kashyap, Sanjay; Woehl, Taylor J.; Liu, Xunpei
  • ACS Nano, Vol. 8, Issue 9
  • DOI: 10.1021/nn502551y

Electron holography of individual DNA molecules
journal, January 1997

  • Fink, Hans-Werner; Schmid, Heinz; Ermantraut, Eugen
  • Journal of the Optical Society of America A, Vol. 14, Issue 9
  • DOI: 10.1364/JOSAA.14.002168

Electron–Water Interactions and Implications for Liquid Cell Electron Microscopy
journal, September 2014

  • Schneider, Nicholas M.; Norton, Michael M.; Mendel, Brian J.
  • The Journal of Physical Chemistry C, Vol. 118, Issue 38
  • DOI: 10.1021/jp507400n

Environmental parameters affect the physical properties of fast-growing magnetosomes
journal, February 2008

  • Faivre, D.; Menguy, N.; Posfai, M.
  • American Mineralogist, Vol. 93, Issue 2-3
  • DOI: 10.2138/am.2008.2678

Local and macroscopic electrostatic interactions in single α-helices
journal, February 2015

  • Baker, Emily G.; Bartlett, Gail J.; Crump, Matthew P.
  • Nature Chemical Biology, Vol. 11, Issue 3
  • DOI: 10.1038/nchembio.1739

Magnetite Biomineralization in Magnetospirillum gryphiswaldense : Time-Resolved Magnetic and Structural Studies
journal, April 2013

  • Fdez-Gubieda, M. Luisa; Muela, Alicia; Alonso, Javier
  • ACS Nano, Vol. 7, Issue 4
  • DOI: 10.1021/nn3059983

Microdosimetry for Nanosecond Pulsed Electric Field Applications: A Parametric Study for a Single Cell
journal, May 2011

  • Merla, C.; Paffi, A.; Apollonio, F.
  • IEEE Transactions on Biomedical Engineering, Vol. 58, Issue 5
  • DOI: 10.1109/TBME.2010.2104150

Electron Holography of Organic and Biological Materials
journal, September 2003


Oversampling smoothness: an effective algorithm for phase retrieval of noisy diffraction intensities
journal, February 2013

  • Rodriguez, Jose A.; Xu, Rui; Chen, Chien-Chun
  • Journal of Applied Crystallography, Vol. 46, Issue 2
  • DOI: 10.1107/S0021889813002471

Electric field induced changes in protein conformation
journal, January 2014

  • Bekard, Innocent; Dunstan, Dave E.
  • Soft Matter, Vol. 10, Issue 3
  • DOI: 10.1039/C3SM52653D

Molecular Dynamics of DNA–Protein Conjugates on Electrified Surfaces: Solutions to the Drift-Diffusion Equation
journal, January 2014

  • Langer, A.; Kaiser, W.; Svejda, M.
  • The Journal of Physical Chemistry B, Vol. 118, Issue 2
  • DOI: 10.1021/jp410640z

Liquid scanning transmission electron microscopy: Nanoscale imaging in micrometers-thick liquids
journal, February 2014


Three-dimensional locations of gold-labeled proteins in a whole mount eukaryotic cell obtained with 3nm precision using aberration-corrected scanning transmission electron microscopy
journal, June 2011

  • Dukes, Madeline J.; Ramachandra, Ranjan; Baudoin, Jean-Pierre
  • Journal of Structural Biology, Vol. 174, Issue 3
  • DOI: 10.1016/j.jsb.2011.03.013

Magnetosome formation in prokaryotes
journal, March 2004

  • Bazylinski, Dennis A.; Frankel, Richard B.
  • Nature Reviews Microbiology, Vol. 2, Issue 3
  • DOI: 10.1038/nrmicro842

Electric Field Effects on Insulin Chain-B Conformation
journal, December 2005

  • Budi, Akin; Legge, F. Sue; Treutlein, Herbert
  • The Journal of Physical Chemistry B, Vol. 109, Issue 47
  • DOI: 10.1021/jp052742q

High-resolution hard x-ray magnetic imaging with dichroic ptychography
journal, August 2016

  • Donnelly, Claire; Scagnoli, Valerio; Guizar-Sicairos, Manuel
  • Physical Review B, Vol. 94, Issue 6
  • DOI: 10.1103/PhysRevB.94.064421

In situ electron holographic study of Ionic liquid
journal, November 2014


Imaging of built-in electric field at a p-n junction by scanning transmission electron microscopy
journal, June 2015

  • Shibata, Naoya; Findlay, Scott D.; Sasaki, Hirokazu
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep10040

Ionic Wave Propagation along Actin Filaments
journal, April 2004


Beyond classical theories
conference, January 2013

  • Kathmann, Shawn M.; Sellner, Bernhard; Alexander, Andrew J.
  • NUCLEATION AND ATMOSPHERIC AEROSOLS: 19th International Conference, AIP Conference Proceedings
  • DOI: 10.1063/1.4803215

XXIst century magnetotherapy
journal, July 2015


Effect of External Electric Field Stress on Gliadin Protein Conformation
journal, July 2013


Holography and coherent diffraction with low-energy electrons: A route towards structural biology at the single molecule level
journal, December 2015


A direct observation of nanometer-size void dynamics in an ultra-thin water film
journal, January 2012

  • Mirsaidov, Utkur; Ohl, Claus-Dieter; Matsudaira, Paul
  • Soft Matter, Vol. 8, Issue 27
  • DOI: 10.1039/c2sm25331c

Rapid magnetosome formation shown by real-time x-ray magnetic circular dichroism
journal, November 2007

  • Staniland, S.; Ward, B.; Harrison, A.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
  • DOI: 10.1073/pnas.0704879104

Supplementary material from "Off-axis electron holography of bacterial cells and magnetic nanoparticles in liquid"
dataset, October 2017

  • Prozorov, Tanya; Almeida, Trevor; Kovács, András
  • figshare-Supplementary information for journal article at DOI: 10.1098/rsif.2017.0464, 1 DOC file (1.44 MB)
  • DOI: 10.6084/m9.figshare.c.3893860

Effects of Electric Field Stress on a β-Amyloid Peptide
journal, January 2009

  • Toschi, Francesca; Lugli, Francesca; Biscarini, Fabio
  • The Journal of Physical Chemistry B, Vol. 113, Issue 1
  • DOI: 10.1021/jp807896g

Low-energy electron holographic imaging of individual tobacco mosaic virions
journal, September 2015

  • Longchamp, Jean-Nicolas; Latychevskaia, Tatiana; Escher, Conrad
  • Applied Physics Letters, Vol. 107, Issue 13
  • DOI: 10.1063/1.4931607

Magnetic Microstructure of Magnetotactic Bacteria by Electron Holography
journal, December 1998


Breaking the diffraction limit of light-sheet fluorescence microscopy by RESOLFT
journal, March 2016

  • Hoyer, Patrick; de Medeiros, Gustavo; Balázs, Bálint
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 13
  • DOI: 10.1073/pnas.1522292113

Electron Holography for the Study of Magnetic Nanomaterials
journal, May 2008

  • Thomas, John Meurig; Simpson, Edward T.; Kasama, Takeshi
  • Accounts of Chemical Research, Vol. 41, Issue 5
  • DOI: 10.1021/ar700225v

Effect of inactivation of poly(hydroxyalkanoates) depolymerase gene on the properties of poly(hydroxyalkanoates) in Pseudomonas resinovorans
journal, October 2003

  • Solaiman, D. K. Y.; Ashby, R. D.; Foglia, T. A.
  • Applied Microbiology and Biotechnology, Vol. 62, Issue 5-6
  • DOI: 10.1007/s00253-003-1317-4

Synthesis of Magnetite Nanoparticles for Bio- and Nanotechnology: Genetic Engineering and Biomimetics of Bacterial Magnetosomes
journal, February 2007

  • Lang, Claus; Schüler, Dirk; Faivre, Damien
  • Macromolecular Bioscience, Vol. 7, Issue 2
  • DOI: 10.1002/mabi.200600235

Modulating protein behaviors on responsive surface by external electric fields: A molecular dynamics study
journal, January 2015


Magnetic microstructure of bacterial magnetite by electron holography [Magnetic microstructure of bacterial magnetite by electron holography]
journal, July 2001


Electric field effects on chignolin conformation
journal, May 2011

  • Astrakas, Loukas; Gousias, Christos; Tzaphlidou, Margaret
  • Journal of Applied Physics, Vol. 109, Issue 9
  • DOI: 10.1063/1.3585867

Magnetosomes Are Cell Membrane Invaginations Organized by the Actin-Like Protein MamK
journal, January 2006


A matter of quantum voltages
journal, October 2014

  • Sellner, Bernhard; Kathmann, Shawn M.
  • The Journal of Chemical Physics, Vol. 141, Issue 18
  • DOI: 10.1063/1.4898797

Differential phase-contrast dark-field electron holography for strain mapping
journal, January 2016


Electron holography of biological samples
journal, April 2008


High-Resolution Electron Microscopy and Spectroscopy of Ferritin in Biocompatible Graphene Liquid Cells and Graphene Sandwiches
journal, February 2014

  • Wang, Canhui; Qiao, Qiao; Shokuhfar, Tolou
  • Advanced Materials, Vol. 26, Issue 21
  • DOI: 10.1002/adma.201306069

Electron holography and AFM studies on styrenic block copolymers and a high impact polystyrene
journal, January 2005

  • Simon, Paul; Adhikari, Rameshwar; Lichte, Hannes
  • Journal of Applied Polymer Science, Vol. 96, Issue 5
  • DOI: 10.1002/app.21600

Specimen preparation for cryogenic coherent X-ray diffraction imaging of biological cells and cellular organelles by using the X-ray free-electron laser at SACLA
journal, May 2016

  • Kobayashi, Amane; Sekiguchi, Yuki; Oroguchi, Tomotaka
  • Journal of Synchrotron Radiation, Vol. 23, Issue 4
  • DOI: 10.1107/S1600577516007736

Electron Holography: Applications to Materials Questions
journal, August 2007


Liquid Scanning Transmission Electron Microscopy: Imaging Protein Complexes in their Native Environment in Whole Eukaryotic Cells
journal, February 2014


Electronic Effects on the Surface Potential at the Vapor−Liquid Interface of Water
journal, December 2008

  • Kathmann, Shawn M.; Kuo, I-Feng William; Mundy, Christopher J.
  • Journal of the American Chemical Society, Vol. 130, Issue 49
  • DOI: 10.1021/ja802851w

Biogenic nanoparticles: production, characterization, and application of bacterial magnetosomes
journal, September 2006


Growth and magnetosome formation by microaerophilic Magnetospirillum strains in an oxygen-controlled fermentor
journal, February 2003