Experimental 3D coherent diffractive imaging from photon-sparse random projections

Giewekemeyer, K.; Aquila, A.; Loh, N. -T. D.; Chushkin, Y.; Shanks, K. S.; Weiss, J. T.; Tate, M. W.; Philipp, H. T.; Stern, S.; Vagovic, P.; Mehrjoo, M.; Teo, C.; Barthelmess, M.; Zontone, F.; Chang, C.; Tiberio, R. C.; Sakdinawat, A.; Williams, G. J.; Gruner, S. M.; Mancuso, A. P.

doi:10.1107/S2052252519002781

Title: Experimental 3D coherent diffractive imaging from photon-sparse random projections

Journal Article · Wed Mar 20 00:00:00 EDT 2019 · IUCrJ

DOI:https://doi.org/10.1107/S2052252519002781· OSTI ID:1617929

Giewekemeyer, K.; Aquila, A.; Loh, N. -T. D.; Chushkin, Y.; Shanks, K. S.; Weiss, J. T.; Tate, M. W.; Philipp, H. T.; Stern, S.; Vagovic, P.; Mehrjoo, M.; Teo, C.; Barthelmess, M.; Zontone, F.; Chang, C.; Tiberio, R. C.; Sakdinawat, A.; Williams, G. J.; Gruner, S. M.; Mancuso, A. P.

The routine atomic resolution structure determination of single particles is expected to have profound implications for probing structure–function relationships in systems ranging from energy-storage materials to biological molecules. Extremely bright ultrashort-pulse X-ray sources – X-ray free-electron lasers (XFELs) – provide X-rays that can be used to probe ensembles of nearly identical nanoscale particles. When combined with coherent diffractive imaging, these objects can be imaged; however, as the resolution of the images approaches the atomic scale, the measured data are increasingly difficult to obtain and, during an X-ray pulse, the number of photons incident on the 2D detector is much smaller than the number of pixels. This latter concern, the signal `sparsity', materially impedes the application of the method. An experimental analog using a conventional X-ray source is demonstrated and yields signal levels comparable with those expected from single biomolecules illuminated by focused XFEL pulses. The analog experiment provides an invaluable cross check on the fidelity of the reconstructed data that is not available during XFEL experiments. Using these experimental data, it is established that a sparsity of order 1.3 × 10 ⁻³ photons per pixel per frame can be overcome, lending vital insight to the solution of the atomic resolution XFEL single-particle imaging problem by experimentally demonstrating 3D coherent diffractive imaging from photon-sparse random projections.

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Research Organization:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0004079; SC0016035; SC0017631; AC02-76SF00515; SC0012704

OSTI ID:: 1617929

Alternate ID(s):: OSTI ID: 1504880

Report Number(s):: BNL-211503-2019-JAAM; IUCRAJ; PII: S2052252519002781

Journal Information:: IUCrJ, Journal Name: IUCrJ Vol. 6 Journal Issue: 3; ISSN 2052-2525

Publisher:: International Union of Crystallography (IUCr)Copyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 19 works

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References (52)

Noise Limits on Reconstructing Diffraction Signals From Random Tomographs Elser, Veit IEEE Transactions on Information Theory, Vol. 55, Issue 10 https://doi.org/10.1109/TIT.2009.2027547	journal	October 2009
Efficient subpixel image registration algorithms Guizar-Sicairos, Manuel; Thurman, Samuel T.; Fienup, James R. Optics Letters, Vol. 33, Issue 2 https://doi.org/10.1364/OL.33.000156	journal	January 2008
Reconstructing three-dimensional protein crystal intensities from sparse unoriented two-axis X-ray diffraction patterns Lan, Ti-Yen; Wierman, Jennifer L.; Tate, Mark W. Journal of Applied Crystallography, Vol. 50, Issue 4 https://doi.org/10.1107/S1600576717006537	journal	June 2017
A minimal view of single-particle imaging with X-ray lasers Loh, N. Duane Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 369, Issue 1647 https://doi.org/10.1098/rstb.2013.0328	journal	July 2014
The Coherent X-ray Imaging Data Bank Maia, Filipe R. N. C. Nature Methods, Vol. 9, Issue 9 https://doi.org/10.1038/nmeth.2110	journal	August 2012
Solving structure with sparse, randomly-oriented x-ray data Philipp, Hugh T.; Ayyer, Kartik; Tate, Mark W. Optics Express, Vol. 20, Issue 12 https://doi.org/10.1364/OE.20.013129	journal	January 2012
The symmetries of image formation by scattering I Theoretical framework Giannakis, Dimitrios; Schwander, Peter; Ourmazd, Abbas Optics Express, Vol. 20, Issue 12 https://doi.org/10.1364/OE.20.012799	journal	January 2012
Femtosecond X-ray protein nanocrystallography Chapman, Henry N.; Fromme, Petra; Barty, Anton Nature, Vol. 470, Issue 7332, p. 73-77 https://doi.org/10.1038/nature09750	journal	February 2011
High-resolution ab initio three-dimensional x-ray diffraction microscopy Chapman, Henry N.; Barty, Anton; Marchesini, Stefano Journal of the Optical Society of America A, Vol. 23, Issue 5 https://doi.org/10.1364/JOSAA.23.001179	journal	January 2006
Expansion-maximization-compression algorithm with spherical harmonics for single particle imaging with x-ray lasers Flamant, Julien; Le Bihan, Nicolas; Martin, Andrew V. Physical Review E, Vol. 93, Issue 5 https://doi.org/10.1103/PhysRevE.93.053302	journal	May 2016
Coherent X-Ray Diffraction Imaging and Characterization of Strain in Silicon-on-Insulator Nanostructures Xiong, Gang; Moutanabbir, Oussama; Reiche, Manfred Advanced Materials, Vol. 26, Issue 46 https://doi.org/10.1002/adma.201304511	journal	June 2014
Solving protein structure from sparse serial microcrystal diffraction data at a storage-ring synchrotron source Lan, Ti-Yen; Wierman, Jennifer L.; Tate, Mark W. IUCrJ, Vol. 5, Issue 5, p. 548-558 https://doi.org/10.1107/S205225251800903X	journal	July 2018
A comprehensive simulation framework for imaging single particles and biomolecules at the European X-ray Free-Electron Laser Yoon, Chun Hong; Yurkov, Mikhail V.; Schneidmiller, Evgeny A. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep24791	journal	April 2016
Considerations for three-dimensional image reconstruction from experimental data in coherent diffractive imaging Lundholm, Ida V.; Sellberg, Jonas A.; Ekeberg, Tomas IUCrJ, Vol. 5, Issue 5 https://doi.org/10.1107/S2052252518010047	journal	September 2018
Serial femtosecond crystallography: the first five years Schlichting, Ilme IUCrJ, Vol. 2, Issue 2, p. 246-255 https://doi.org/10.1107/S205225251402702X	journal	February 2015
Protein crystal structure from non-oriented, single-axis sparse X-ray data Wierman, Jennifer L.; Lan, Ti-Yen; Tate, Mark W. IUCrJ, Vol. 3, Issue 1 https://doi.org/10.1107/S2052252515018795	journal	January 2016
Single-particle imaging without symmetry constraints at an X-ray free-electron laser Rose, Max; Bobkov, Sergey; Ayyer, Kartik IUCrJ, Vol. 5, Issue 6, p. 727-736 https://doi.org/10.1107/S205225251801120X	journal	September 2018
Coherent diffraction of single Rice Dwarf virus particles using hard X-rays at the Linac Coherent Light Source Munke, Anna; Andreasson, Jakob; Aquila, Andrew Scientific Data, Vol. 3, Issue 1 https://doi.org/10.1038/sdata.2016.64	journal	August 2016
Correlations in Scattered X-Ray Laser Pulses Reveal Nanoscale Structural Features of Viruses Kurta, Ruslan P.; Donatelli, Jeffrey J.; Yoon, Chun Hong Physical Review Letters, Vol. 119, Issue 15, Article No. 158102 https://doi.org/10.1103/PhysRevLett.119.158102	journal	October 2017
Cryptotomography: Reconstructing 3D Fourier Intensities from Randomly Oriented Single-Shot Diffraction Patterns Loh, N. D.; Bogan, M. J.; Elser, V. Physical Review Letters, Vol. 104, Issue 22 https://doi.org/10.1103/PhysRevLett.104.225501	journal	June 2010
Invited Article: A unified evaluation of iterative projection algorithms for phase retrieval Marchesini, S. Review of Scientific Instruments, Vol. 78, Issue 1 https://doi.org/10.1063/1.2403783	journal	January 2007
Optimal mapping of x-ray laser diffraction patterns into three dimensions using routing algorithms Kassemeyer, Stephan; Jafarpour, Aliakbar; Lomb, Lukas Physical Review E, Vol. 88, Issue 4 https://doi.org/10.1103/PhysRevE.88.042710	journal	October 2013
Structure from fleeting illumination of faint spinning objects in flight Fung, Russell; Shneerson, Valentin; Saldin, Dilano K. Nature Physics, Vol. 5, Issue 1 https://doi.org/10.1038/nphys1129	journal	November 2008
Potential for biomolecular imaging with femtosecond X-ray pulses Neutze, Richard; Wouts, Remco; van der Spoel, David Nature, Vol. 406, Issue 6797 https://doi.org/10.1038/35021099	journal	August 2000
Coherent soft X-ray diffraction imaging of coliphage PR772 at the Linac coherent light source Reddy, Hemanth K. N.; Yoon, Chun Hong; Aquila, Andrew Scientific Data, Vol. 4, Issue 1 https://doi.org/10.1038/sdata.2017.79	journal	June 2017
Common arc method for diffraction pattern orientation Bortel, Gábor; Tegze, Miklós Acta Crystallographica Section A Foundations of Crystallography, Vol. 67, Issue 6 https://doi.org/10.1107/S0108767311036269	journal	October 2011
X-ray image reconstruction from a diffraction pattern alone Marchesini, S.; He, H.; Chapman, H. N. Physical Review B, Vol. 68, Issue 14 https://doi.org/10.1103/PhysRevB.68.140101	journal	October 2003
Start-to-end simulation of single-particle imaging using ultra-short pulses at the European X-ray Free-Electron Laser Fortmann-Grote, Carsten; Buzmakov, Alexey; Jurek, Zoltan IUCrJ, Vol. 4, Issue 5 https://doi.org/10.1107/S2052252517009496	journal	September 2017
Orientation determination in single-particle x-ray coherent diffraction imaging experiments Yefanov, O. M.; Vartanyants, I. A. Journal of Physics B: Atomic, Molecular and Optical Physics, Vol. 46, Issue 16 https://doi.org/10.1088/0953-4075/46/16/164013	journal	August 2013
Experimental strategies for imaging bioparticles with femtosecond hard X-ray pulses Daurer, Benedikt J.; Okamoto, Kenta; Bielecki, Johan IUCrJ, Vol. 4, Issue 3, p. 251-262 https://doi.org/10.1107/S2052252517003591	journal	April 2017
Fourier shell correlation threshold criteria van Heel, Marin; Schatz, Michael Journal of Structural Biology, Vol. 151, Issue 3 https://doi.org/10.1016/j.jsb.2005.05.009	journal	September 2005
Single-particle XFEL 3D reconstruction of ribosome-size particles based on Fourier slice matching: requirements to reach subnanometer resolution Nakano, Miki; Miyashita, Osamu; Jonic, Slavica Journal of Synchrotron Radiation, Vol. 25, Issue 4 https://doi.org/10.1107/S1600577518005568	journal	May 2018
Reconstruction from limited single-particle diffraction data via simultaneous determination of state, orientation, intensity, and phase Donatelli, Jeffrey J.; Sethian, James A.; Zwart, Peter H. Proceedings of the National Academy of Sciences, Vol. 114, Issue 28 https://doi.org/10.1073/pnas.1708217114	journal	June 2017
A Medium-Format, Mixed-Mode Pixel Array Detector for Kilohertz X-ray Imaging Tate, M. W.; Chamberlain, D.; Green, K. S. Journal of Physics: Conference Series, Vol. 425, Issue 6 https://doi.org/10.1088/1742-6596/425/6/062004	journal	March 2013
Dragonfly : an implementation of the expand–maximize–compress algorithm for single-particle imaging Ayyer, Kartik; Lan, Ti-Yen; Elser, Veit Journal of Applied Crystallography, Vol. 49, Issue 4 https://doi.org/10.1107/S1600576716008165	journal	June 2016
Real-Space x-ray tomographic reconstruction of randomly oriented objects with sparse data frames Ayyer, Kartik; Philipp, Hugh T.; Tate, Mark W. Optics Express, Vol. 22, Issue 3 https://doi.org/10.1364/OE.22.002403	journal	January 2014
Diffraction imaging of single particles and biomolecules Huldt, G.; Szőke, A.; Hajdu, J. Journal of Structural Biology, Vol. 144, Issue 1-2 https://doi.org/10.1016/j.jsb.2003.09.025	journal	October 2003
Three-dimensional coherent diffractive imaging on non-periodic specimens at the ESRF beamline ID10 Chushkin, Y.; Zontone, F.; Lima, E. Journal of Synchrotron Radiation, Vol. 21, Issue 3 https://doi.org/10.1107/S1600577514003440	journal	March 2014
Reconstruction algorithm for single-particle diffraction imaging experiments Loh, Ne-Te Duane; Elser, Veit Physical Review E, Vol. 80, Issue 2 https://doi.org/10.1103/PhysRevE.80.026705	journal	August 2009
A multiple-common-lines method to determine the orientation of snapshot diffraction patterns from single particles Zhou, Liang; Zhang, Tian-Yi; Liu, Zhong-Chuan Acta Crystallographica Section A Foundations and Advances, Vol. 70, Issue 4 https://doi.org/10.1107/S2053273314007049	journal	June 2014
Structure determination from single molecule X-ray scattering with three photons per image von Ardenne, Benjamin; Mechelke, Martin; Grubmüller, Helmut Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-04830-4	journal	June 2018
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
Iterative phasing for fluctuation X-ray scattering Donatelli, Jeffrey J.; Zwart, Peter H.; Sethian, James A. Proceedings of the National Academy of Sciences, Vol. 112, Issue 33 https://doi.org/10.1073/pnas.1513738112	journal	August 2015
Atomic structure of a single large biomolecule from diffraction patterns of random orientations Tegze, Miklós; Bortel, Gábor Journal of Structural Biology, Vol. 179, Issue 1 https://doi.org/10.1016/j.jsb.2012.04.014	journal	July 2012
The linac coherent light source single particle imaging road map Aquila, A.; Barty, A.; Bostedt, C. Structural Dynamics, Vol. 2, Issue 4 https://doi.org/10.1063/1.4918726	journal	July 2015
Three-dimensional reconstruction for coherent diffraction patterns obtained by XFEL Nakano, Miki; Miyashita, Osamu; Jonic, Slavica Journal of Synchrotron Radiation, Vol. 24, Issue 4 https://doi.org/10.1107/S1600577517007767	journal	June 2017
Single molecule imaging using X-ray free electron lasers Barty, Anton Current Opinion in Structural Biology, Vol. 40 https://doi.org/10.1016/j.sbi.2016.11.017	journal	October 2016
XFELs for structure and dynamics in biology Spence, J. C. H. IUCrJ, Vol. 4, Issue 4 https://doi.org/10.1107/S2052252517005760	journal	May 2017
Phase-retrieval stagnation problems and solutions Fienup, J. R.; Wackerman, C. C. Journal of the Optical Society of America A, Vol. 3, Issue 11 https://doi.org/10.1364/JOSAA.3.001897	journal	January 1986
A comprehensive simulation framework for imaging single particles and biomolecules at the European X-ray Free-Electron Laser Yoon, Chun Hong; Yurkov, Mikhail; Schneidmiller, Evgeny Alexanrdovich Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2016-01805	text	January 2016
Coherent diffraction of single Rice Dwarf virus particles using hard X-rays at the Linac Coherent Light Source Munke, Anna; Andreasson, Jakob; Aquila, Andrew Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2016-02771	text	January 2016
Cryptotomography: Reconstructing 3D Fourier Intensities from Randomly Oriented Single-Shot Diffraction Patterns Loh, N. D.; Bogan, M. J.; Elser, V. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/phppubdb-14441	text	January 2010

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Experimental 3D Coherent Diffractive Imaging from photon-sparse random projections Giewekemeyer, Giewekemeyer; K., K. Coherent X-ray Imaging Data Bank (Lawrence Berkeley National Laboratory); European XFEL https://doi.org/10.11577/1498641	dataset	January 2019