MATERIALS SCIENCE

Atomic-resolution transmissionelectron microscopy of electronbeam–sensitive crystalline materialsDaliang 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 difficultapplications of transmission electron microscopy (TEM).The challenges are manifold,including the acquisition of images with extremely low beam doses, the time-constrainedsearch for crystal zone axes, the precise image alignment, and the accurate determination ofthe defocus value.We develop a suite of methods to fulfill these requirements and acquireatomic-resolution TEM images of several metal organic frameworks that are generallyrecognized as highly sensitive to electron beams.The high image resolution allows us toidentify individual metal atomic columns, various types of surface termination, and benzenerings in the organic linkers.We also apply our methods to other electron beam–sensitivematerials, 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 awide range ofmaterials thatare easily damaged by the electron beams (2–5).Metal organic frameworks (MOFs), which havedesignable porous structures and fascinatingproperties (6–8), represent a typical example ofelectron beam–sensitive materials. During thefew attempts to image MOFs by HRTEM, onlythe primary channels could be resolved by thelimited resolution as a result of beam damage(2, 9–11).Themechanisms of beamdamage are complex

and vary with the material, primarily includingknock-on damage, heating effects, and radiolysis(3, 4, 12). One means of alleviating beam damageis to reduce the energy of electron beam.HRTEMwith low accelerating voltages has successfullyimaged carbon nanotube and graphene (13–15).However, the use of low-energy electrons resultsin poor image resolution and a short penetrationdepth, and only prevents knock-on damage.Similarly, the use of cryo-TEM only lessens theheating damage to a certain degree (11). An al-ternative, in-principle more general solutionto this issue is to acquire the HRTEM imageswith a sufficiently low electron dose to capturethe structure before damage occurs. Althoughthis idea is straightforward, it is difficult to re-

alize because it requires an extremely sensi-tive camera to record acceptable images withonly a few electrons per pixel. Conventionalcameras cannot produce images with a suffi-cient signal-to-noise ratio under such low-doseconditions.Direct-detection electron-counting (DDEC) cam-

eras have an exceptionally high detective quan-tum efficiency and enable HRTEM at ultralowelectron doses (16, 17). Taking advantage of this,structural biologists have boosted the voxel reso-lution for protein structures by using cryo-TEM(18). In the field of materials science, however, thepotential of DDEC cameras inHRTEM imaging ofelectron beam–sensitivematerials remains largelyunexplored, owing to some practical obstacles.First, unlike the single-particle cryo-TEM thatreconstructs a protein structure from randomlyoriented particles, for crystallinematerials imagesshould be acquired along specific directions, i.e.,along the zone axes of the lattice. With beam-sensitive specimens, the process of finding a zoneaxis must be accomplished very quickly to min-imize the beam irradiation. Second, the electron-countingmode is capable of producing successiveshort-exposure images, but the images must beprecisely aligned to fully restore thehigh-resolutioninformation. Third, it is impossible to acquire afocus series of a beam-sensitive material, evenwhen using a DDEC camera, and thus the in-terpretation of the image is difficult unless anaccurate defocus value can be determined. Wereported the use of a DDEC camera to image aMOF material (ZIF-8) with an ultralow electrondose, in which the zone-axis image was obtainedby sampling a large number of randomly orientedcrystals (19). However, this is an inefficient trial-and-error process, and success is not guaranteed.In this work, we develop a suite of methods toovercome these obstacles, advancing theHRTEMof beam-sensitive materials to a nearly routineprocess.

To design the quantitative HRTEM conditionsforMOFs,we first evaluated their stabilities undera 300-kV accelerated electron beam. The resultsreveal that MOFs began to lose their crystallin-ity when the cumulative electron dose reached10 to 20 e− Å−2, as determined by the fading ofthe electron diffraction (ED) spots (fig. S1). Thesevalues set the upper limits of the cumulative elec-tron dose for both locating a zone axis and thesubsequent image acquisition. In our experiments,we used a DDEC camera to acquire images ata reasonably high magnification of 55,000 toachieve atomic resolution (pixel size: 0.57 Å by0.57 Å) with electron doses of 2 to 4 e− per pixel(6 to 12 e− Å−2). Therefore, the maximum elec-tron dose that can be used to find a zone axis isless than 10 e− Å−2. The conventional, manualmethod for aligning a zone axis does not meetthis threshold, because it requires time-consuming,iterative toggles between the diffraction and im-agingmodes, often causing the total electron doseto reach hundreds of electrons per Å2.We developed a simple program to achieve a

direct, one-step alignment of the zone axis (figs.S2 and S3). When the electron beam incidencedeviates from a zone axis by an angleϕ, the zero-order Laue zone of the lattice intersects with theEwald sphere, forming an arc in the ED that ispart of the Laue circle. The radius of the Lauecircle is approximately equal to sin(ϕ) × (1/l),where l is the wavelength of the beam. Ourprogram first identifies a Laue circle by analyzingthe distribution of reflections from an off-axis EDpattern. Unlike an earlier software of automaticzone-axis alignment (20) that estimates the crystalorientation by evaluating the intensities of re-flections, our program determines the Laue circlefrom the positions of reflections to avoid the in-fluence of structure factors or dynamic effects.Once the Laue circle is identified, ϕ is deter-mined by its radius and l. The program then de-composes ϕ into two components, ϕa and ϕb,which correspond to two tilting angles aroundthe a-tilt and b-tilt axes of the double-tilt TEMholder, based on the predetermined directionsof the two tilting axes. By applying the program-calculated tilting anglesϕa andϕb, we candirectlytilt the crystal from the initial orientation to alignwith the zone axis. The whole process requires theacquisition of only two EDs, one for determiningthe Laue circle and the other for confirming theon-axis orientation; the electron beam is blankedin between while the program does its calcula-tions, and the total dose consumed is far below1 e−/Å2. This method requires that the initialcrystal orientation is close to a zone axis (−5° <ϕ < 5°); otherwise, there are very few reflectionsobserved in ED, making the identification of aLaue circle difficult. In practice, the probabilityof seeing a Laue circle is >10% in randomlyoriented powder samples.HRTEM of electron beam–sensitive materials

often suffers from a beam-induced specimenmotion that results in blurred images. Whenusing a DDEC camera, this issue can be over-come by breaking the total exposure into a stackof successive short-exposure images (frames),

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1King Abdullah University of Science and Technology (KAUST),Imaging and Characterization Core Lab, Thuwal 23955-6900,Saudi Arabia. 2KAUST, Advanced Membranes and PorousMaterials Center, Physical Sciences and Engineering Division,Thuwal 23955-6900, Saudi Arabia. 3KAUST, KAUST CatalysisCenter, Physical Sciences and Engineering Division, Thuwal23955-6900, Saudi Arabia.*Corresponding author. Email: daliang.zhang@kaust.edu.sa (D.Z.);kun.li@kaust.edu.sa (K.L.); yu.han@kaust.edu.sa (Y.H.) †Presentaddress: Department of Chemical Engineering, Zhejiang University ofTechnology, Hangzhou 310014, P.R. China.

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Zhang et al., Science 359, 675–679 (2018) 9 February 2018 2 of 5

Fig. 1. Alignment of an image stack using the“amplitude filter.” (A) A single frame and(B) the corresponding FT in an HRTEM imagestack (120 frames in total) acquired for UiO-66along the <011> zone axis. (C) The FT amplitudepattern formed by summing up the FTamplitudecomponent of all frames. (D) Modified FT of asingle frame by adopting filtered amplitudesfrom (C). (E) An amplitude-filtered single framethat is produced by inverse FT of (D). (F) Theimage-drift profile determined from filteredframes. (G) The drift-corrected image based on(F). (H) The drift-corrected image by cross-correlation, where the image stack is 1 × 1 × 10binned to enhance the signal-to-noise ratio.(I) Uncorrected image formed by directlysumming up all the frames. In (G) to (I), thecorresponding FTs are shown as insets; the halfcircles represent the frequency of 2 Å. In (G), alocal area is magnified to highlight the observed14 –4 4 reflection (d = 1.4 Å).

Fig. 2. HRTEM images of UiO-66acquired from different zone axes.(A) <001>, (B) <011>, (C) <111>,and (D) <013>. The top, middle, andbottom rows show raw images,denoised images, and FTs of the rawimages, respectively. The half circlesin the FTs represent 2 Å. In alldirections, there are reflectionsobserved beyond the circle, indicatingthat the information transfer isless than 2 Å. As an example, the10 –6 6 reflection (d = 1.6 Å) ishighlighted in (B).

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on the condition that the drift between framescan be precisely corrected by image alignment.In principle, the exposure of each frame shouldbe as short as possible to minimize specimenmotion and statistical errors from the detector.However, beam-sensitive materials require a lowelectron dose rate to avoid structural damage,and consequently, short exposure times result invery noisy frames with a poor signal-to-noiseratio that cannot be aligned by using the commonmethods based on feature matching or phasecorrelation. To increase the signal to noise, sev-eral successive frames can be merged into one,which is equal to using longer exposure and thusdetrimental to image resolution, especially whenthe specimen motion is severe. Image filterscan also increase the signal to noise to facilitateimage alignment, but the existing filters do notwork well with high noise levels (fig. S4).A general principle of image alignment is to

decompose a real-space image into componentsof different spatial frequencies in the reciprocalspace by Fourier transform (FT). Image drift

can be determined from the “phases” variation inthe FTs. The difficulty in aligning noisy imageslies in the poor signal-to-noise ratio that affectsthe accuracy of phase determination. We hypoth-esize that the impact of noise can be minimizedby selectively analyzing pixels in the FT withstrong amplitudes, because phase determinationof weak pixels is more easily influenced by noiseand prone to errors. On the basis of this hypoth-esis, we developed an “amplitude filter” to confinethe phase analysis to “reliable” strong-amplitudepixels (figs. S5 and S6).Unlike the common methods that deal with

the weak signals of individual frames, the “am-plitude filter” starts by integrating the FTs of allthe frames in an image stack to pinpoint thestrong-amplitude pixels. The workflow is illus-trated in Fig. 1 with an HRTEM image stack ofMOF UiO-66 (21). With an extremely low dose(0.033 e−/pixel) (Fig. 1A), even the reflections aredifficult to identify in the FTof each frame (Fig. 1B).We summed the FT amplitude components fromall of the frames in the stack, as the reflections have

invariable coordinates in the FTs, irrespective ofimage drift. As shown in Fig. 1C, the “hidden”reflections emerged in the summed FT amplitudepattern (we call it “amplitude pattern” because itdoes not contain phase information). We filteredout background and weak pixels that have am-plitudes lower than a set threshold from theamplitude pattern. The “amplitudes” of the re-maining pixels were combined with the “phases”from the original FT of each frame to generatea series of modified FTs (Fig. 1D), followed byinverse FTs to generate a series of filtered images(Fig. 1E). Finally, the image drift was calculatedby using iterative cross-correlation based on thefiltered images (Fig. 1F), and this informationwas used to align the original images in the stack.The drift-corrected, summed image shows richhigh-resolution structural details, as evidencedby the appearance of the 1.4 Å reflection in theFT (Fig. 1G). By contrast, the cross-correlationwithout our “amplitude filter” could not correctlyalign this image stack until it was 1 × 1 × 10binned, which led to a marked reduction in

Zhang et al., Science 359, 675–679 (2018) 9 February 2018 3 of 5

Fig. 3. HRTEM of thermally treated UiO-66. (A) Drift-corrected HRTEMimage of a truncated octahedral UiO-66 crystal and an ultrathin piece ofcrystal with the same <011> orientation. (B) CTF-corrected denoised imagefrom the ultrathin crystal [area 2 in (A)], showing triangular channels,individual Zr atomic columns, and the BDC linkers.The benzene rings in theBDC linkers are indicated by the arrows. Overlays are simulated projectedpotential maps and a projected structural model of UiO-66 for comparison.(C) A truncation surface [area 1 in (A)], showing crystal growth stepsinvolving small {100} facets and {111} facets (labeled in blue and yellow,respectively).The white arrows indicate “kink” positions between {100} and

{111} facets. (D) Ligand-terminated {111} surface: (left) structural model;(middle) processed HRTEM image by real-space averaging of 5 motifs fromarea 3 in (A); (right) the averaged image displayed in rainbow colors toincrease the visibility of the ligand contrast. (E) Ligand-free (metal-terminated) {100}/{111} kink: (left) structural model; (middle) processedHRTEM image by real-space averaging of seven motifs from area 1 in (A);(right) the averaged image displayed in rainbow colors. (F and G) Thestructure model (left) and the processed HRTEM image (right) of the (F)hydroxylated and (G) dehydroxylated Zr clusters featuring different Zr-Zrdistances.The image processing details are shown in fig. S13.

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image resolution in the direction of the imagedrift (Fig. 1H). The result of merging all of theframes without drift correction is shown in Fig.1I for comparison.Wecannowstudy variousMOFswithTEMalong

different zone axes and restore high-resolutioninformation fromtheobtained images.Results fromMOFUiO-66 are presented in Fig. 2. The successfulacquisition ofHRTEM images from four zone axes,<001>, <011>, <111>, and<013>, demonstrates theeffectivenessof ourmethod for zone-axis alignment.FTs of these images show that the informationtransfer is <2Å in all directions (Fig. 2), confirmingthe efficacy of our method for image alignment.The contrast inHRTEM images varies with the

specimen thickness and defocus, making a singleimage difficult to interpret directly. A commonpractice inHRTEM is to acquire a series of imageswith different defocuses for structure reconstruc-tion (22, 23). However, thismethod is not suitablefor MOFs because it is impossible to acquiremultiple images without causing structural dam-age, even when using the low-dose conditions. Onthe other hand, the very low framework density ofMOFs greatly decreases their effective scatteringthickness; therefore, we can safely apply theweak-phase object approximation to MOFs for a widerange of thicknesses up to ~100nm. Consequently,a single image can be mademore interpretable bycorrecting the “contrast inversion” caused by thecontrast transfer function (CTF) of the objectivelens, if the absolute defocus of the image is known(24). Here we propose that we can take advantageof the “instability” of MOFs to determine thedefocus. Specifically, after an HRTEM image iscaptured, we prolong the beam irradiation todeliberately destroy the crystalline structure andacquire a focus series of this amorphized area(fig. S7). Using establishedmethods (22), we candetermine the absolute defocus value of eachimage in the series and, thus, that of the HRTEMimage of MOF for CTF correction.The success of our methodology has been

demonstrated in a case study, in which anHRTEMimage of UiO-66 along the <011> axis was ac-quired, aligned, and CTF-corrected by usingthe methods described above. The sample washeated at 300°C under vacuum for 10 hours toremove the solvent molecules before HRTEM.The imaged area contains a truncated octahedralcrystal with an ultrathin piece of crystal protrud-ing from its lower right corner (Fig. 3A). In theCTF-corrected and denoised image (Fig. 3B andfig. S8), triangular channels encompassed by threemetal clusters and three 1,4-benzenedicarboxylicacids (BDCs) are identified, and atomic columnsof Zr are distinguished within the Zr6O8 clusters,in good agreement with the crystal structure ofUiO-66. The benzene rings with face-on config-urations in the BDC linkers are resolved (Fig. 3Band fig. S8). In addition to the bulk structure,our image reveals detailed local structures. Atthe truncation surface of the octahedral crystalthat corresponds to the fast-growing {100} planes,the crystal growth steps are identified as a num-ber of small {100} and {111} facets (Fig. 3C).Furthermore, the high resolution allows us to

investigate the surface termination of this crystal.In the CTF-corrected image, the outermost layerof Zr clusters have dark contrast and can beidentified at the crystal surfaces, where the or-ganic linkers are hardly visible because of theweak contrast associated with the low atomicnumbers. We performed real-space averagingalong the crystal surface to enhance the signal-to-noise ratio (fig. S9). The results reveal thecoexistence of ligand-free (metal-exposing) andligand-capped surfaces: The major exposed {111}surface terminates with BDC linkers (Fig. 3D);in contrast, the small truncation surface (growthsteps) exposes Zr clusters at the kink positionsbetween {100} and {111} facets (Fig. 3E).It has been speculated that upon heating to

300°C, the octahedral ZrO4(OH)4 clusters in UiO-66 undergo dehydroxylation, forming distortedZr6O6 clusters (25). In a <110> projection, thisdistortion gives rise to increased Zr-Zr distancesalong the in-plane <110> direction (fig. S10). How-ever, the random orientation of this distortionmakes it difficult to verify by conventional char-acterizations. Using HRTEM, we observed thesubtle structural change inUiO-66 associatedwithdehydroxylation (figs. S11 to S13). As revealed inthe images, the as-synthesized UiO-66 containsonly one type of Zr cluster with uniform Zr-Zrdistances of 3.34 Å, whereas the heated UiO-66contains two types of Zr clusters; one is the sameas the cluster in the as-synthesized sample, and theother has larger Zr-Zr distances of 3.89 Å (Fig. 3, Fand G, and fig. S12). This result supports spec-

ulation that the Zr clusters in UiO-66 becomedistorted upon heating (25). The appearance of asmall number of undistorted clusters (Zr-Zr: 3.34 Å)in the heated UiO-66 (fig. S13) was likely causedby partial rehydroxylation during the TEM samplepreparation process. We note that the exact valuesof the Zr-Zr distancemeasured byHRTEMare notvery accurate because of the pixel size limitations.HRTEM images of MOFs ZIF-8 and HKUST-1

(26) and a germanosilicate zeolite are presentedin figs. S14 and S15, which show good matchingwith the corresponding crystal structures afterCTF correction. We also successfully acquiredHRTEM images of the organic-inorganic hybridperovskite CH3NH3PbBr3, which has emergedas an optoelectronic material and is known tobe very sensitive to electron beams. The hybridperovskites show anomalous current-voltage (I-V)hysteresis in photovoltaic applications (27). Ferro-electric effect (28) and ion migration (29) havebeen posited to be likely causes for the hysteresis.Our image reveals that CH3NH3PbBr3 crystalscontain ordered nanometer-sized domains withoff-centered CH3NH3 cations that have differingorientations. In the two typical domains highlightedin Fig. 4, the CH3NH3 cations exhibit normal andparallel configurations (relative to the projectiondirection), giving rise to in-plane and out-of-planeelectric dipoles, respectively. This observationimplies the ferroelectric order in this material.In this study, we have developed a suite of

methodologies that enable atomic-resolutionTEMimaging of electron beam–sensitive crystalline

Zhang et al., Science 359, 675–679 (2018) 9 February 2018 4 of 5

Fig. 4. HRTEM of organic-inorganic hybrid perovskite CH3NH3PbBr3. (A) CTF-correcteddenoised HRTEM image. The raw image is shown in fig. S16. The squares highlight two ordereddomains with off-centered CH3NH3 cations that have differing orientations. (B and C) The structuralmodel (left) (30) and the simulated projected potential map (right) of CH3NH3PbBr3 with differentCH3NH3 orientations, corresponding to region 1 and 2 in (A), respectively. In (B) and (C), the off-centered CH3NH3 cations exhibit normal and parallel configurations (relative to the projectiondirection), giving rise to in-plane and out-of-plane electric dipoles, respectively.

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materials, which have traditionally been con-sidered unsuitable for TEM characterization.Withthis capability, we can observe the local structuresof MOFs and other fragile materials, substantiallyexpanding the range of applications for HRTEM.It is worth noting that our method for zone-axisalignment not only reduces the electron dose, butalso enhances the precision of alignment. Its appli-cation is not limited to beam-sensitivematerials; itis particularly useful for aligning nanosized crystals.Likewise, our method for image alignment canbe generally applied to various noisy images withperiodic features. This study facilitates investiga-tions in a wide variety of “unstable” materialsusing HRTEM.

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ACKNOWLEDGMENTS

We thank M. Pan and O. Terasaki for helpful discussions. Thiswork was supported by King Abdullah University of Science andTechnology through Competitive Research Grant (URF/1/2570-01)and Center Competitive Funding (FCC/1/1972-19). HRTEM imagespresented in this paper and the two programs used for zone-axisalignment and image alignment are archived in a data repository(https://zenodo.org/record/1133206) for verification purposes only.Interested readers can download the programs after agreeing withthe terms and conditions stated there. D.Z., Y.Z., K.L., and Y.H.are inventors on United States Provisional patent applications(62/490,967 and 62/490,968) submitted by King AbdullahUniversity of Science and Technology that cover the methods forcrystal zone–axis alignment and image alignment.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/359/6376/675/suppl/DC1Materials and MethodsFigs. S1 to S16Table S1References (31–41)

12 June 2017; resubmitted 29 September 2017Accepted 27 December 2017Published online 18 January 201810.1126/science.aao0865

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materialssensitive crystalline−Atomic-resolution transmission electron microscopy of electron beam

Daliang Zhang, Yihan Zhu, Lingmei Liu, Xiangrong Ying, Chia-En Hsiung, Rachid Sougrat, Kun Li and Yu Han

originally published online January 18, 2018DOI: 10.1126/science.aao0865 (6376), 675-679.359Science 

, this issue p. 675Science(metal-exposing) and ligand-capped surfaces in UiO-66 crystals.frameworks. With this approach, they could see the benzene rings in a UiO-66 linker and the coexistence of ligand-freeelectron-counting camera with ways to limit the overall electron dose to analyze delicate materials such as metal organic

combined a state-of-the-art direct-detectionet al.lead to damage, particularly in fragile materials. Zhang many materials. However, the need for high beam doses, especially as a sample is rotated to find the crystal axes, can

High-resolution transmission electron microscopy is an invaluable tool for looking at the crystalline structures ofCrystallography of sensitive materials

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