Abstract
Liquid phase (or liquid cell) transmission electron microscopy (LP-TEM) has been established as a powerful tool for observing dynamic processes in liquids at nanometer to atomic length scales. However, the simple act of observation using electrons irreversibly alters the nature of the sample. A clear understanding of electron-beam-driven processes during LP-TEM is required to interpret in situ observations and utilize the electron beam as a stimulus to drive nanoscale dynamic processes. In this article, we discuss recent advances toward understanding, quantifying, mitigating, and harnessing electron-beam-driven chemical processes occurring during LP-TEM. We highlight progress in several research areas, including modeling electron-beam-induced radiolysis near interfaces, electron-beam-induced nanocrystal formation, and radiation damage of soft materials and biomolecules.
Similar content being viewed by others
References
M.J. Williamson, R.M. Tromp, P.M. Vereecken, R. Hull, F.M. Ross, Nat. Mater. 2, 532 (2003).
F.M. Ross, Science 350, 9886 (2015).
N. de Jonge, D.B. Peckys, G.J. Kremers, D.W. Piston, Proc. Natl. Acad. Sci. U.S.A. 106, 2159 (2009).
N. de Jonge, F.M. Ross, Nat. Nanotechnol. 6, 695 (2011).
H.M. Zheng, R.K. Smith, Y.W. Jun, C. Kisielowski, U. Dahmen, A.P. Alivisatos, Science 324, 1309 (2009).
J. Lyu, X. Gong, S.-J. Lee, K. Gnanasekaran, X. Zhang, M.C. Wasson, X. Wang, P. Bai, X. Guo, N.C. Gianneschi, O.K. Farha, J. Am. Chem. Soc. 142, 4609 (2020).
M. Gu, L.R. Parent, B.L. Mehdi, R.R. Unocic, M.T. McDowell, R.L. Sacci, W. Xu, J.G. Connell, P. Xu, P. Abellan, X. Chen, Y. Zhang, D.E. Perea, J.E. Evans, L.J. Lauhon, J.-G. Zhang, J. Liu, N.D. Browning, Y. Cui, I. Arslan, C.-M. Wang, Nano Lett. 13, 6106 (2013).
R.L. Sacci, J.M. Black, N. Balke, N.J. Dudney, K.L. More, R.R. Unocic, Nano Lett. 15, 2011 (2015).
A. Ianiro, H. Wu, M.M.J. van Rijt, M.P. Vena, A.D.A. Keizer, A.C.C. Esteves, R. Tuinier, H. Friedrich, N.A.J.M. Sommerdijk, J.P. Patterson, Nat. Chem. 11, 320 (2019).
A.J. Swallow, Radiation Chemistry: An Introduction (Wiley, New York, 1973).
E. Collinson, A.J. Swallow, Chem. Rev. 56, 471 (1956).
J.M. Grogan, N.M. Schneider, F.M. Ross, H.H. Bau, Nano Lett. 14, 359 (2014).
N.M. Schneider, M.M. Norton, B.J. Mendel, J.M. Grogan, F.M. Ross, H.H. Bau, J. Phys. Chem. C 118, 22373 (2014).
J. Cookman, V. Hamilton, L.S. Price, S.R. Hall, U. Bangert, Nanoscale 12, 4636 (2020).
P. Abellan, B.L. Mehdi, L.R. Parent, M. Gu, C. Park, W. Xu, Y.H. Zhang, I. Arslan, J.G. Zhang, C.M. Wang, J.E. Evans, N.D. Browning, Nano Lett. 14, 1293 (2014).
T.J. Woehl, P. Abellan, J. Microsc. 265, 135 (2017).
E. Sutter, K. Jungjohann, S. Bliznakov, A. Courty, E. Maisonhaute, S. Tenney, P. Sutter, Nat. Commun. 5, 4946 (2014).
T. Gupta, N.M. Schneider, J.H. Park, D. Steingart, F.M. Ross, Nanoscale 10, 7702 (2018).
R.R. Unocic, A.R. Lupini, A.Y. Borisevich, D.A. Cullen, S.V. Kalinin, S. Jesse, Nanoscale 8, 15581 (2016).
M. den Heijer, I. Shao, A. Radisic, M.C. Reuter, F.M. Ross, APL Mater. 2, 022101 (2014).
J.E. Evans, K.L. Jungjohann, N.D. Browning, I. Arslan, Nano Lett. 11, 2809 (2011).
T.J. Woehl, K.L. Jungjohann, J.E. Evans, I. Arslan, W.D. Ristenpart, N.D. Browning, Ultramicroscopy 127, 53 (2013).
K.L. Jungjohann, S. Bliznakov, P.W. Sutter, E.A. Stach, E.A. Sutter, Nano Lett. 13, 2964 (2013).
P. Abellan, T.J. Woehl, L.R. Parent, N.D. Browning, J.E. Evans, I. Arslan, Chem. Commun. 50, 4873 (2014).
T.H. Moser, H. Mehta, C. Park, R.T. Kelly, T. Shokuhfar, J.E. Evans, Sci. Adv. 4, eaaq1202 (2018).
T. Gupta, N.M. Schneider, J.H. Park, D. Steingart, F.M. Ross, Nanoscale 10, 7702 (2018).
J.H. Park, N.M. Schneider, J.M. Grogan, M.C. Reuter, H.H. Bau, S. Kodambaka, F.M. Ross, Nano Lett. 15, 5314 (2015).
A. Hutzler, T. Schmutzler, M.P.M. Jank, R. Branscheid, T. Unruh, E. Spiecker, L. Frey, Nano Lett. 18, 7222 (2018).
S.M. Rehn, M.R. Jones, ACS Energy Lett. 3, 1269 (2018).
M.R. Hauwiller, J.C. Ondry, C.M. Chan, P. Khandekar, J. Yu, A.P. Alivisatos, J. Am. Chem. Soc. 141, 4428 (2019).
T.J. Woehl, J.E. Evans, L. Arslan, W.D. Ristenpart, N.D. Browning, ACS Nano 6, 8599 (2012).
T.J. Woehl, C. Park, J.E. Evans, I. Arslan, W.D. Ristenpart, N.D. Browning, Nano Lett. 14, 373 (2014).
D. Alloyeau, W. Dachraoui, Y. Javed, H. Belkahla, G. Wang, H. Lecoq, S. Ammar, O. Ersen, A. Wisnet, F. Gazeau, C. Ricolleau, Nano Lett. 15, 2574 (2015).
H.G. Liao, L.K. Cui, S. Whitelam, H.M. Zheng, Science 336, 1011 (2012).
P. Abellan, T.H. Moser, I.T. Lucas, J.W. Grate, J.E. Evans, N.D. Browning, RSC Adv. 7, 3831 (2017).
P. Abellan, L.R. Parent, N. Al Hasan, C. Park, I. Arslan, A.M. Karim, J.E. Evans, N.D. Browning, Langmuir 32, 1468 (2016).
T.J. Woehl, Chem. Mater. (2020), doi:10.1021/acs.chemmater.0c01360.
M. Wang, C. Park, T.J. Woehl, Chem. Mater. 30, 7727 (2018).
T.H. Moser, H. Mehta, C. Park, R.T. Kelly, T. Shokuhfar, J.E. Evans, Sci. Adv. 4, eaaq1202 (2018).
N. Ahmad, G. Wang, J. Nelayah, C. Ricolleau, D. Alloyeau, Nano Lett. 17, 4194 (2017).
J. Sung, B.K. Choi, B. Kim, B.H. Kim, J. Kim, D. Lee, S. Kim, K. Kang, T. Hyeon, J. Park, J. Am. Chem. Soc. 141, 18395 (2019).
M. Sun, B. Yu, M. Hong, Z. Li, F. Lyu, X. Li, Z. Li, X. Wei, Z. Zhang, Y. Zhang, Q. Chen, Small 16, 1906435 (2020).
P. Liu, Q. Chen, Y. Ito, J.H. Han, S.F. Chu, X.D. Wang, K.M. Reddy, S.X. Song, A. Hirata, M.W. Chen, Nano Lett. 20, 1944 (2020).
M.R. Hauwiller, L.B. Frechette, M.R. Jones, J.C. Ondry, G.M. Rotskoff, P. Geissler, A.P. Alivisatos, Nano Lett. 18, 5731 (2018).
S. Wu, M. Li, Y. Sun, Angew. Chem. Int. Ed. Engl. 58, 8995 (2019).
M. Wang, T.U. Dissanayake, C. Park, K. Gaskell, T.J. Woehl, J. Am. Chem. Soc. 141, 13516 (2019).
H.-W. Cheng, S. Yan, J. Li, J. Wang, L. Wang, Z. Skeete, S. Shan, C.-J. Zhong, ACS Appl. Mater. Interfaces 10, 40348 (2018).
B. Dahlgren, M.A. Sabatino, C. Dispenza, M. Jonsson, Macromol. Theory Simul. 29, 1900046 (2020).
P. Ulański Zainuddin, J.M. Rosiak, Radiat. Phys. Chem. 46, 913 (1995).
P. Ulański, I. Janik, J.M. Rosiak, Radiat. Phys. Chem. 52, 289 (1998).
K.H. Nagamanasa, H. Wang, S. Granick, Adv. Mater. 29, 1703555 (2017).
Y.Z. Liu, X.M. Lin, Y.G. Sun, T. Rajh, J. Am. Chem. Soc. 135, 3764 (2013).
T.J. Woehl, T. Prozorov, J. Phys. Chem. C 119, 21261 (2015).
A. Verch, M. Pfaff, N. de Jonge, Langmuir 31, 6956 (2015).
A.W. Girotti, Free Radic. Biol. Med. 1, 87 (1985).
E. Niki, Y. Yoshida, Y. Saito, N. Noguchi, Biochem. Biophys. Res. Commun. 338, 668 (2005).
E.N. Frankel, Prog. Lipid Res. 23, 197 (1984).
G. Stark, J. Membr. Biol. 205, 1 (2005).
H.W. Gardner, Free Radic. Biol. Med. 7, 65 (1989).
G. Stark, Biochim. Biophys. Acta Biomembr. 1071, 103 (1991).
E.N. Frankel, Chem. Phys. Lipids 44, 73 (1987).
M.A. Acosta-Elias, A.J. Burgara-Estrella, J.A. Sarabia-Sainz, E. Silva-Campa, A. Angulo-Molina, K.J. Santacruz-Gomez, B. Castaneda, D. Soto-Puebla, A.I. Ledesma-Osuna, R. Melendrez-Amavizca, M. Pedroza-Montero, Int. J. Radiat. Biol. 93, 1306 (2017).
J. Wong-Ekkabut, Z. Xu, W. Triampo, I.M. Tang, D.P. Tieleman, L. Monticelli, Biophys. J. 93, 4225 (2007).
T. Nakazawa, S. Nagatsuka, Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 38, 537 (1980).
T.H. Moser, T. Shokuhfar, J.E. Evans, Micron 117, 8 (2019).
T.H. Moser, H. Mehta, C. Park, R.T. Kelly, T. Shokuhfar, J.E. Evans, Sci. Adv. 4, eaaq1202 (2018).
T. Woehl, S. Kashap, M. Sánchez-Quesada, C. Jiménez López, T. Perez-Gonzalez, D. Faivre, D. Trubytsyn, D. Bazylinski, T. Prozorov, Microsc. Microanal. 20, 1510 (2014).
T.J. Woehl, S. Kashyap, E. Firlar, T. Perez-Gonzalez, D. Faivre, D. Trubitsyn, D.A. Bazylinski, T. Prozorov, Sci. Rep. 4, 6854 (2014).
C. Barth, G. Stark, Biochim. Biophys. Acta Biomembr. 1066, 54 (1991).
L. Kunz, U. Zeidler, K. Haegele, M. Przybylski, G. Stark, Biochemistry 34, 11895 (1995).
C. Barth, G. Stark, M. Wilhelm, Biophys. J. 64, 92 (1993).
I.D. Desai, A.L. Tappel, J. Lipid Res. 4, 204 (1963).
H. Schuessler, K. Schilling, Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 45, 267 (1984).
E.R. Stadtman, R.L. Levine, Amino Acids 25, 207 (2003).
W.M. Garrison, Chem. Rev. 87, 381 (1987).
K. Uchida, Y. Kato, S. Kawakishi, Biochem. Biophys. Res. Commun. 169, 265 (1990).
A. Amici, R.L. Levine, L. Tsai, E.R. Stadtman, J. Biol. Chem. 264, 3341 (1989).
G. Taborsky, Biochemistry 12, 1341 (1973).
K. Uchida, S. Kawakishi, FEBS Lett. 332, 208 (1993).
R.C. Armstrong, A.J. Swallow, Radiat. Res. 40 (1969).
P. Koufen, G. Stark, Biochim. Biophys. Acta Mol. Basis Dis. 1501, 44 (2000).
P. Koufen, A. RüCk, D. Brdiczka, S. Wendt, T. Wallimann, G. Stark, Biochem. J. 344, 413 (1999).
K. Hitschke, R. Bühler, H.J. Apell, G. Stark, FEBS Lett. 353, 297 (1994).
J.I. Kourie, Am. J. Physiol. 275, C1 (1998).
V. Cecarini, J. Gee, E. Fioretti, M. Amici, M. Angeletti, A.M. Eleuteri, J.N. Keller, Biochim. Biophys. Acta 1773, 93 (2007).
M.A. Touve, A.S. Carlini, N.C. Gianneschi, Nat. Commun. 10, 4837 (2019).
N.M. Schneider, M.M. Norton, B.J. Mendel, J.M. Grogan, F.M. Ross, H.H. Bau, J. Phys. Chem. C 118, 22373 (2014).
S.V. Tokalov, A.S. Iagunov, Radiat. Environ. Biophys. 50, 265 (2011).
H.S. Eom, H.S. Park, G.E. You, J.Y. Kim, S.Y. Nam, Int. J. Radiat. Biol. 93, 1207 (2017).
S. Acharya, N.N. Bhat, P. Joseph, G. Sanjeev, B. Sreedevi, Y. Narayana, Radiat. Environ. Biophys. 50, 253 (2011).
M.B. Sowa, L.E. Kathmann, B.A. Holben, B.D. Thrall, G.A. Kimmel, Radiat. Res. 164, 677 (2005).
Acknowledgments
J.E.E. and T.M. were supported by the Environmental Molecular Sciences Laboratory (EMSL) Strategic Science Area Project No. 50427. EMSL (grid.436923.9) is a US Department of Energy Office of Science User Facility sponsored by the Office of Biological and Environmental Research. T.J.W. acknowledges support from the Petroleum Research Fund (Grant No. 61111-DNI10).
Appendix
Appendix
Taylor J. Woehl-has been an assistant professor in the Department of Chemical and Biomolecular Engineering at the University of Maryland, College Park, since 2016. He leads the Nanoscale Assembly and Electron Microscopy Laboratory. He obtained his PhD degree in chemical engineering from the University of California, Davis, in 2013. He was an assistant research scientist at Ames Laboratory from 2013 to 2014. He received a National Research Council Postdoctoral Fellowship from 2014 to 2016, working in the Material Measurement Laboratory at the National Institute of Standards Technology on new low-voltage transmission electron and ion-microscopy techniques. His research focuses on nanochemistry, colloidal assembly, liquid phase transmission electron microscopy, and protein aggregation. Woehl can be reached by email at tjwoehl@umd.edu.
Trevor Moser-is a research scientist in the Environmental Molecular Sciences Laboratory at Pacific Northwest National Laboratory (PNNL). He received his PhD degree in biochemistry and molecular biology from Michigan Technological University in 2018. He completed postdoctoral research at PNNL. His research interests include characterizing radiation damage of biological materials in liquid-phase transmission electron microscopy, as well as the structural determination of proteins and macromolecular complexes using cryo-EM tomography. Moser can be reached by email at trevor.moser@pnnl.gov.
James Evans-has been a staff scientist in the Environmental Molecular Sciences Laboratory at Pacific Northwest National Laboratory since 2011. He received his PhD degree in biochemistry and molecular biology from the University of California, Davis, in 2007. He completed postdoctoral research at Lawrence Livermore National Laboratory, and then moved to the University of California, Davis, in 2009, where he was awarded his first grant as principal investigator for the development of in situ transmission electron microscopy (TEM). His research focuses on advancing dynamic microscopy, liquid phase TEM, and cryo-EM bioimaging applications. Evans can be reached by email at james.evans@pnnl.gov.
Frances M. Ross-has been the Ellen Swallow Richards Professor in the Department of Materials Science and Engineering at the Massachusetts Institute of Technology since 2018. She received her BA degree in physics and her PhD degree in materials science from Cambridge University, UK. She completed postdoctoral research at AT&T Bell Laboratories. She was a staff scientist at the National Center for Electron Microscopy at Lawrence Berkeley National Laboratory, and a research staff member at the IBM T.J. Watson Research Center. Her research focuses on nanostructure self-assembly, liquid cell microscopy, epitaxy, and electrochemical processes. Ross can be reached by email at fmross@mit.edu.
Rights and permissions
About this article
Cite this article
Woehl, T.J., Moser, T., Evans, J.E. et al. Electron-beam-driven chemical processes during liquid phase transmission electron microscopy. MRS Bulletin 45, 746–753 (2020). https://doi.org/10.1557/mrs.2020.227
Published:
Issue Date:
DOI: https://doi.org/10.1557/mrs.2020.227