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We acknowledge valuable financial support from the Air Force
Office of Scientific Research (AFOSR) under award FA9550-16-1-
0109, the AFOSR Multidisciplinary University Research Initiative
grant FA9550-15-1-0037, and from Canada’s National Research
Council and Natural Sciences and Engineering Research Council.
The authors declare no competing financial interests. G.V. thanks
B. Schmidt for insightful discussions. All data needed to evaluate
the conclusions in the paper are present in the paper and/or the
Materials and Methods
Figs. S1 to S6
19 September 2017; accepted 21 December 2017
electron microscopy of electron
beam–sensitive crystalline materials
Daliang Zhang,1 Yihan Zhu,2† Lingmei Liu,2 Xiangrong Ying,2 Chia-En Hsiung,2
Rachid Sougrat,1 Kun Li,1 Yu Han2,3*
High-resolution imaging of electron beam–sensitive materials is one of the most difficult
applications of transmission electron microscopy (TEM). The challenges are manifold,
including the acquisition of images with extremely low beam doses, the time-constrained
search for crystal zone axes, the precise image alignment, and the accurate determination of
the defocus value. We develop a suite of methods to fulfill these requirements and acquire
atomic-resolution TEM images of several metal organic frameworks that are generally
recognized as highly sensitive to electron beams. The high image resolution allows us to
identify individual metal atomic columns, various types of surface termination, and benzene
rings in the organic linkers. We also apply our methods to other electron beam–sensitive
materials, including the organic-inorganic hybrid perovskite CH3NH3PbBr3.
Understanding the fundamental structure- property relationships in functional mate- rials is the essence of materials science. High-resolution TEM (HRTEM) is a pow- erful tool for structure characterization (1).
However, there are a wide range of materials that
are easily damaged by the electron beams (2–5).
Metal organic frameworks (MOFs), which have
designable porous structures and fascinating
properties (6–8), represent a typical example of
electron beam–sensitive materials. During the
few attempts to image MOFs by HRTEM, only
the primary channels could be resolved by the
limited resolution as a result of beam damage
The mechanisms of beam damage are complex
and vary with the material, primarily including
knock-on damage, heating effects, and radiolysis
(3, 4, 12). One means of alleviating beam damage
is to reduce the energy of electron beam. HRTEM
with low accelerating voltages has successfully
imaged carbon nanotube and graphene (13–15).
However, the use of low-energy electrons results
in poor image resolution and a short penetration
depth, and only prevents knock-on damage.
Similarly, the use of cryo-TEM only lessens the
heating damage to a certain degree (11). An al-
ternative, in-principle more general solution
to this issue is to acquire the HRTEM images
with a sufficiently low electron dose to capture
the structure before damage occurs. Although
this idea is straightforward, it is difficult to re-
alize because it requires an extremely sensi-
tive camera to record acceptable images with
only a few electrons per pixel. Conventional
cameras cannot produce images with a suffi-
cient signal-to-noise ratio under such low-dose
Direct-detection electron-counting (DDEC) cameras have an exceptionally high detective quantum efficiency and enable HRTEM at ultralow
electron doses (16, 17). Taking advantage of this,
structural biologists have boosted the voxel resolution for protein structures by using cryo-TEM
(18). In the field of materials science, however, the
potential of DDEC cameras in HRTEM imaging of
electron beam–sensitive materials remains largely
unexplored, owing to some practical obstacles.
First, unlike the single-particle cryo-TEM that
reconstructs a protein structure from randomly
oriented particles, for crystalline materials images
should be acquired along specific directions, i.e.,
along the zone axes of the lattice. With beam-sensitive specimens, the process of finding a zone
axis must be accomplished very quickly to minimize the beam irradiation. Second, the electron-counting mode is capable of producing successive
short-exposure images, but the images must be
precisely aligned to fully restore the high-resolution
information. Third, it is impossible to acquire a
focus series of a beam-sensitive material, even
when using a DDEC camera, and thus the interpretation of the image is difficult unless an
accurate defocus value can be determined. We
reported the use of a DDEC camera to image a
MOF material (ZIF-8) with an ultralow electron
dose, in which the zone-axis image was obtained
by sampling a large number of randomly oriented
crystals (19). However, this is an inefficient trial-and-error process, and success is not guaranteed.
In this work, we develop a suite of methods to
overcome these obstacles, advancing the HRTEM
of beam-sensitive materials to a nearly routine
To design the quantitative HRTEM conditions
for MOFs, we first evaluated their stabilities under
a 300-kV accelerated electron beam. The results
reveal that MOFs began to lose their crystallinity when the cumulative electron dose reached
10 to 20 e− Å−2, as determined by the fading of
the electron diffraction (ED) spots (fig. S1). These
values set the upper limits of the cumulative electron dose for both locating a zone axis and the
1King Abdullah University of Science and Technology (KAUST),
Imaging and Characterization Core Lab, Thuwal 23955-6900,
Saudi Arabia. 2KAUST, Advanced Membranes and Porous
Materials Center, Physical Sciences and Engineering Division,
Thuwal 23955-6900, Saudi Arabia. 3KAUST, KAUST Catalysis
Center, Physical Sciences and Engineering Division, Thuwal
23955-6900, Saudi Arabia.
*Corresponding author. Email: email@example.com (D.Z.);
firstname.lastname@example.org (K.L.); email@example.com (Y.H.) †Present
address: Department of Chemical Engineering, Zhejiang University of
Technology, Hangzhou 310014, P.R. China.