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Title: X-ray linear dichroic ptychography

Abstract

Biominerals such as seashells, coral skeletons, bone, and tooth enamel are optically anisotropic crystalline materials with unique nanoscale and microscale organization that translates into exceptional macroscopic mechanical properties, providing inspiration for engineering new and superior biomimetic structures. Using Seriatopora aculeata coral skeleton as a model, here, we experimentally demonstrate X-ray linear dichroic ptychography and map the c-axis orientations of the aragonite (CaCO3) crystals. Linear dichroic phase imaging at the oxygen K-edge energy shows strong polarization-dependent contrast and reveals the presence of both narrow (<35°) and wide (>35°) c-axis angular spread in the coral samples. These X-ray ptychography results are corroborated by four-dimensional (4D) scanning transmission electron microscopy (STEM) on the same samples. Evidence of co-oriented, but disconnected, corallite subdomains indicates jagged crystal boundaries consistent with formation by amorphous nanoparticle attachment. We expect that the combination of X-ray linear dichroic ptychography and 4D STEM could be an important multimodal tool to study nano-crystallites, interfaces, nucleation, and mineral growth of optically anisotropic materials at multiple length scales.

Authors:
 [1];  [1];  [1];  [2];  [2];  [3];  [4];  [5];  [4]; ORCiD logo [6];  [2];  [2]; ORCiD logo [7];  [1]
  1. Univ. of California, Los Angeles, CA (United States); Univ. of Colorado, Boulder, CO (United States)
  2. Univ. of Colorado, Boulder, CO (United States); National Inst. of Standards and Technology (NIST), Boulder, CO (United States). JILA
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
  5. Univ. of Wisconsin, Madison, WI (United States)
  6. Univ. of Colorado, Boulder, CO (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS); Univ. of California, Berkeley, CA (United States)
  7. Univ. of Wisconsin, Madison, WI (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Los Angeles, CA (United States); Univ. of Wisconsin, Madison, WI (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division; National Science Foundation (NSF); USDOE National Nuclear Security Administration (NNSA)
OSTI Identifier:
1831072
Grant/Contract Number:  
SC0010378; FG02-07ER15899; AC02-05CH11231; NA0003864; DMR-1603192; DMR 1548924
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 118; Journal Issue: 3; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS; coherent diffractive imaging; ptychography; X-ray linear dichroism; biominerals; 4D scanning transmission electron microscopy

Citation Formats

Lo, Yuan Hung, Zhou, Jihan, Rana, Arjun, Morrill, Drew, Gentry, Christian, Enders, Bjoern, Yu, Young-Sang, Sun, Chang-Yu, Shapiro, David A., Falcone, Roger W., Kapteyn, Henry C., Murnane, Margaret M., Gilbert, Pupa A., and Miao, Jianwei. X-ray linear dichroic ptychography. United States: N. p., 2021. Web. doi:10.1073/pnas.2019068118.
Lo, Yuan Hung, Zhou, Jihan, Rana, Arjun, Morrill, Drew, Gentry, Christian, Enders, Bjoern, Yu, Young-Sang, Sun, Chang-Yu, Shapiro, David A., Falcone, Roger W., Kapteyn, Henry C., Murnane, Margaret M., Gilbert, Pupa A., & Miao, Jianwei. X-ray linear dichroic ptychography. United States. https://doi.org/10.1073/pnas.2019068118
Lo, Yuan Hung, Zhou, Jihan, Rana, Arjun, Morrill, Drew, Gentry, Christian, Enders, Bjoern, Yu, Young-Sang, Sun, Chang-Yu, Shapiro, David A., Falcone, Roger W., Kapteyn, Henry C., Murnane, Margaret M., Gilbert, Pupa A., and Miao, Jianwei. Tue . "X-ray linear dichroic ptychography". United States. https://doi.org/10.1073/pnas.2019068118. https://www.osti.gov/servlets/purl/1831072.
@article{osti_1831072,
title = {X-ray linear dichroic ptychography},
author = {Lo, Yuan Hung and Zhou, Jihan and Rana, Arjun and Morrill, Drew and Gentry, Christian and Enders, Bjoern and Yu, Young-Sang and Sun, Chang-Yu and Shapiro, David A. and Falcone, Roger W. and Kapteyn, Henry C. and Murnane, Margaret M. and Gilbert, Pupa A. and Miao, Jianwei},
abstractNote = {Biominerals such as seashells, coral skeletons, bone, and tooth enamel are optically anisotropic crystalline materials with unique nanoscale and microscale organization that translates into exceptional macroscopic mechanical properties, providing inspiration for engineering new and superior biomimetic structures. Using Seriatopora aculeata coral skeleton as a model, here, we experimentally demonstrate X-ray linear dichroic ptychography and map the c-axis orientations of the aragonite (CaCO3) crystals. Linear dichroic phase imaging at the oxygen K-edge energy shows strong polarization-dependent contrast and reveals the presence of both narrow (<35°) and wide (>35°) c-axis angular spread in the coral samples. These X-ray ptychography results are corroborated by four-dimensional (4D) scanning transmission electron microscopy (STEM) on the same samples. Evidence of co-oriented, but disconnected, corallite subdomains indicates jagged crystal boundaries consistent with formation by amorphous nanoparticle attachment. We expect that the combination of X-ray linear dichroic ptychography and 4D STEM could be an important multimodal tool to study nano-crystallites, interfaces, nucleation, and mineral growth of optically anisotropic materials at multiple length scales.},
doi = {10.1073/pnas.2019068118},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 3,
volume = 118,
place = {United States},
year = {Tue Jan 12 00:00:00 EST 2021},
month = {Tue Jan 12 00:00:00 EST 2021}
}

Works referenced in this record:

Single mimivirus particles intercepted and imaged with an X-ray laser
journal, February 2011

  • Seibert, M. Marvin; Ekeberg, Tomas; Maia, Filipe R. N. C.
  • Nature, Vol. 470, Issue 7332
  • DOI: 10.1038/nature09748

Three-Dimensional Visualization of a Human Chromosome Using Coherent X-Ray Diffraction
journal, January 2009


Orientation of Chemisorbed Molecules from Surface-Absorption Fine-Structure Measurements: CO and NO on Ni(100)
journal, August 1981


Imaging whole Escherichia coli bacteria by using single-particle x-ray diffraction
journal, December 2002

  • Miao, J.; Hodgson, K. O.; Ishikawa, T.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 1
  • DOI: 10.1073/pnas.232691299

Simultaneous cryo X-ray ptychographic and fluorescence microscopy of green algae
journal, February 2015

  • Deng, Junjing; Vine, David J.; Chen, Si
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1413003112

Growth and structure in abalone shell
journal, January 2005


GENFIRE: A generalized Fourier iterative reconstruction algorithm for high-resolution 3D imaging
journal, September 2017


Observing crystal nucleation in four dimensions using atomic electron tomography
journal, June 2019


Electron tomography at 2.4-ångström resolution
journal, March 2012

  • Scott, M. C.; Chen, Chien-Chun; Mecklenburg, Matthew
  • Nature, Vol. 483, Issue 7390
  • DOI: 10.1038/nature10934

Coherent X-ray diffraction imaging of strain at the nanoscale
journal, April 2009

  • Robinson, Ian; Harder, Ross
  • Nature Materials, Vol. 8, Issue 4
  • DOI: 10.1038/nmat2400

Near-edge X-ray refraction fine structure microscopy
journal, February 2017

  • Farmand, Maryam; Celestre, Richard; Denes, Peter
  • Applied Physics Letters, Vol. 110, Issue 6
  • DOI: 10.1063/1.4975377

Extending the methodology of X-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens
journal, July 1999

  • Miao, Jianwei; Charalambous, Pambos; Kirz, Janos
  • Nature, Vol. 400, Issue 6742
  • DOI: 10.1038/22498

Architecture of Columnar Nacre, and Implications for Its Formation Mechanism
journal, June 2007


A New Paradigm for Biomineral Formation: Mineralization via an Amorphous Liquid-Phase Precursor
journal, January 2003

  • Olszta, Matthew; Odom, Damian; Douglas, Elliot
  • Connective Tissue Research, Vol. 44, Issue 1
  • DOI: 10.1080/713713604

Ptychographic Imaging of Nano-Materials at the Advanced Light Source with the Nanosurveyor Instrument
journal, June 2017


Beyond crystallography: Diffractive imaging using coherent x-ray light sources
journal, April 2015


Self-consistent ion-by-ion growth model for kinetic isotopic fractionation during calcite precipitation
journal, June 2012

  • Nielsen, Laura C.; DePaolo, Donald J.; De Yoreo, James J.
  • Geochimica et Cosmochimica Acta, Vol. 86
  • DOI: 10.1016/j.gca.2012.02.009

Crystal growth kinetics as an architectural constraint on the evolution of molluscan shells
journal, September 2019

  • Schoeppler, Vanessa; Lemanis, Robert; Reich, Elke
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 41
  • DOI: 10.1073/pnas.1907229116

Three-dimensional magnetization structures revealed with X-ray vector nanotomography
journal, July 2017

  • Donnelly, Claire; Guizar-Sicairos, Manuel; Scagnoli, Valerio
  • Nature, Vol. 547, Issue 7663
  • DOI: 10.1038/nature23006

High-resolution ab initio three-dimensional x-ray diffraction microscopy
journal, January 2006

  • Chapman, Henry N.; Barty, Anton; Marchesini, Stefano
  • Journal of the Optical Society of America A, Vol. 23, Issue 5
  • DOI: 10.1364/JOSAA.23.001179

MANTiS : a program for the analysis of X-ray spectromicroscopy data
journal, July 2014


Nacre tablet thickness records formation temperature in modern and fossil shells
journal, February 2017

  • Gilbert, Pupa U. P. A.; Bergmann, Kristin D.; Myers, Corinne E.
  • Earth and Planetary Science Letters, Vol. 460
  • DOI: 10.1016/j.epsl.2016.11.012

High-Resolution Scanning X-ray Diffraction Microscopy
journal, July 2008


Deciphering chemical order/disorder and material properties at the single-atom level
journal, February 2017

  • Yang, Yongsoo; Chen, Chien-Chun; Scott, M. C.
  • Nature, Vol. 542, Issue 7639
  • DOI: 10.1038/nature21042

Ptychography – a label free, high-contrast imaging technique for live cells using quantitative phase information
journal, August 2013

  • Marrison, Joanne; Räty, Lotta; Marriott, Poppy
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep02369

Chemical composition mapping with nanometre resolution by soft X-ray microscopy
journal, September 2014


Impact of ocean acidification on crystallographic vital effect of the coral skeleton
journal, July 2019


Biomineralization of calcium carbonates and their engineered applications: a review
journal, January 2013

  • Dhami, Navdeep K.; Reddy, M. Sudhakara; Mukherjee, Abhijit
  • Frontiers in Microbiology, Vol. 4
  • DOI: 10.3389/fmicb.2013.00314

Revealing crystalline domains in a mollusc shell single-crystalline prism
journal, July 2017

  • Mastropietro, F.; Godard, P.; Burghammer, M.
  • Nature Materials, Vol. 16, Issue 9
  • DOI: 10.1038/nmat4937

Quantitative imaging of anisotropic material properties with vectorial ptychography
journal, January 2018

  • Ferrand, Patrick; Baroni, Arthur; Allain, Marc
  • Optics Letters, Vol. 43, Issue 4
  • DOI: 10.1364/OL.43.000763

Nanoscale Imaging of Mineral Crystals inside Biological Composite Materials Using X-Ray Diffraction Microscopy
journal, January 2008


Stable isotopes ( 13C and  15N) of organic matrix from coral skeleton
journal, January 2005

  • Muscatine, L.; Goiran, C.; Land, L.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 5
  • DOI: 10.1073/pnas.0408921102

X-ray ptychography
journal, December 2017


On Biomineralization
book, July 1989


Quantitative biological imaging by ptychographic x-ray diffraction microscopy
journal, December 2009

  • Giewekemeyer, K.; Thibault, P.; Kalbfleisch, S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 2
  • DOI: 10.1073/pnas.0905846107

Coral Skeleton Construction: A Physiochemically Dominated Process
journal, April 1986


Mollusc larval shell formation: amorphous calcium carbonate is a precursor phase for aragonite
journal, August 2002

  • Weiss, Ingrid Maria; Tuross, Noreen; Addadi, Lia
  • Journal of Experimental Zoology, Vol. 293, Issue 5
  • DOI: 10.1002/jez.90004

Internal structure of sponge glass fiber revealed by ptychographic nanotomography
journal, April 2016

  • Birkbak, Mie E.; Guizar-Sicairos, Manuel; Holler, Mirko
  • Journal of Structural Biology, Vol. 194, Issue 1
  • DOI: 10.1016/j.jsb.2016.02.006

A phase retrieval algorithm for shifting illumination
journal, November 2004

  • Rodenburg, J. M.; Faulkner, H. M. L.
  • Applied Physics Letters, Vol. 85, Issue 20
  • DOI: 10.1063/1.1823034

Polarized X-ray scattering reveals non-crystalline orientational ordering in organic films
journal, April 2012

  • Collins, B. A.; Cochran, J. E.; Yan, H.
  • Nature Materials, Vol. 11, Issue 6
  • DOI: 10.1038/nmat3310

Measurement of c-axis angular orientation in calcite (CaCO3) nanocrystals using X-ray absorption spectroscopy
journal, June 2011

  • Gilbert, P. U. P. A.; Young, A.; Coppersmith, S. N.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 28
  • DOI: 10.1073/pnas.1107917108

Correlative cellular ptychography with functionalized nanoparticles at the Fe L-edge
journal, July 2017

  • Gallagher-Jones, Marcus; Dias, Carlos Sato Baraldi; Pryor, Alan
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/s41598-017-04784-5

Phase retrieval from the magnitude of the Fourier transforms of nonperiodic objects
journal, January 1998

  • Miao, J.; Sayre, D.; Chapman, H. N.
  • Journal of the Optical Society of America A, Vol. 15, Issue 6
  • DOI: 10.1364/JOSAA.15.001662

Crystal nucleation and growth of spherulites demonstrated by coral skeletons and phase-field simulations
journal, June 2020


Spherulitic Growth of Coral Skeletons and Synthetic Aragonite: Nature’s Three-Dimensional Printing
journal, June 2017


Nanosurveyor 2: A Compact Instrument for Nano-Tomography at the Advanced Light Source
journal, June 2017


Quantitative Imaging of Single, Unstained Viruses with Coherent X Rays
journal, October 2008


An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy
journal, March 2009

  • Howells, M. R.; Beetz, T.; Chapman, H. N.
  • Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3
  • DOI: 10.1016/j.elspec.2008.10.008

Ptychographic X-ray nanotomography quantifies mineral distributions in human dentine
journal, March 2015

  • Zanette, I.; Enders, B.; Dierolf, M.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep09210

Amorphous calcium carbonate particles form coral skeletons
journal, August 2017

  • Mass, Tali; Giuffre, Anthony J.; Sun, Chang-Yu
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
  • DOI: 10.1073/pnas.1707890114

Ptychographic X-ray computed tomography at the nanoscale
journal, September 2010

  • Dierolf, Martin; Menzel, Andreas; Thibault, Pierre
  • Nature, Vol. 467, Issue 7314
  • DOI: 10.1038/nature09419

Coherently aligned nanoparticles within a biogenic single crystal: A biological prestressing strategy
journal, December 2017

  • Polishchuk, Iryna; Bracha, Avigail Aronhime; Bloch, Leonid
  • Science, Vol. 358, Issue 6368
  • DOI: 10.1126/science.aaj2156

X-ray Linear Dichroism Microscopy
journal, November 1993


Polarimetry of Pinctada fucata nacre indicates myostracal layer interrupts nacre structure
journal, February 2017

  • Metzler, Rebecca A.; Jones, Joshua A.; D'Addario, Anthony J.
  • Royal Society Open Science, Vol. 4, Issue 2
  • DOI: 10.1098/rsos.160893

Oxygen Spectroscopy and Polarization-Dependent Imaging Contrast (PIC)-Mapping of Calcium Carbonate Minerals and Biominerals
journal, May 2014

  • DeVol, Ross T.; Metzler, Rebecca A.; Kabalah-Amitai, Lee
  • The Journal of Physical Chemistry B, Vol. 118, Issue 28
  • DOI: 10.1021/jp503700g

From particle attachment to space-filling coral skeletons
journal, November 2020

  • Sun, Chang-Yu; Stifler, Cayla A.; Chopdekar, Rajesh V.
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 48
  • DOI: 10.1073/pnas.2012025117

Further improvements to the ptychographical iterative engine
journal, January 2017


The hidden structure of human enamel
journal, September 2019


Impact-resistant nacre-like transparent materials
journal, June 2019


Mapping the 3D orientation of nanocrystals and nanostructures in human bone: Indications of novel structural features
journal, June 2020

  • Grünewald, Tilman A.; Liebi, Marianne; Wittig, Nina K.
  • Science Advances, Vol. 6, Issue 24
  • DOI: 10.1126/sciadv.aba4171

High speed, direct detection 1k Frame-Store CCD sensor for synchrotron radiation
conference, October 2011

  • Doering, Dionisio; Andresen, Nord; Contarato, Devis
  • 2011 IEEE Nuclear Science Symposium and Medical Imaging Conference (2011 NSS/MIC), 2011 IEEE Nuclear Science Symposium Conference Record
  • DOI: 10.1109/NSSMIC.2011.6154370

Correlating the three-dimensional atomic defects and electronic properties of two-dimensional transition metal dichalcogenides
journal, March 2020


Bioinspired structural materials
journal, October 2014

  • Wegst, Ulrike G. K.; Bai, Hao; Saiz, Eduardo
  • Nature Materials, Vol. 14, Issue 1
  • DOI: 10.1038/nmat4089

A New Paradigm for Biomineral Formation: Mineralization via an Amorphous Liquid-Phase Precursor
journal, January 2003

  • Olszta, Matthew J.; Odom, Damian J.; Douglas, Elliot P.
  • Connective Tissue Research, Vol. 44, Issue 1
  • DOI: 10.1080/03008200390181852

Correlative 3D x-ray fluorescence and ptychographic tomography of frozen-hydrated green algae
journal, November 2018

  • Deng, Junjing; Lo, Yuan Hung; Gallagher-Jones, Marcus
  • Science Advances, Vol. 4, Issue 11
  • DOI: 10.1126/sciadv.aau4548

Internal structure of sponge glass fiber revealed by ptychographic nanotomography
journal, April 2016

  • Birkbak, Mie E.; Guizar-Sicairos, Manuel; Holler, Mirko
  • Journal of Structural Biology, Vol. 194, Issue 1
  • DOI: 10.1016/j.jsb.2016.02.006

Oxygen Spectroscopy and Polarization-Dependent Imaging Contrast (PIC)-Mapping of Calcium Carbonate Minerals and Biominerals
journal, May 2014

  • DeVol, Ross T.; Metzler, Rebecca A.; Kabalah-Amitai, Lee
  • The Journal of Physical Chemistry B, Vol. 118, Issue 28
  • DOI: 10.1021/jp503700g

Extending the methodology of X-ray crystallography to allow imaging of micrometre-sized non-crystalline specimens
journal, July 1999

  • Miao, Jianwei; Charalambous, Pambos; Kirz, Janos
  • Nature, Vol. 400, Issue 6742
  • DOI: 10.1038/22498

Three-dimensional magnetization structures revealed with X-ray vector nanotomography
journal, July 2017

  • Donnelly, Claire; Guizar-Sicairos, Manuel; Scagnoli, Valerio
  • Nature, Vol. 547, Issue 7663
  • DOI: 10.1038/nature23006

Chemical composition mapping with nanometre resolution by soft X-ray microscopy
journal, September 2014


Stable isotopes ( 13C and  15N) of organic matrix from coral skeleton
journal, January 2005

  • Muscatine, L.; Goiran, C.; Land, L.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 5
  • DOI: 10.1073/pnas.0408921102

High-Resolution Scanning X-ray Diffraction Microscopy
journal, July 2008


X-ray Linear Dichroism Microscopy
journal, November 1993


Impact-resistant nacre-like transparent materials
journal, June 2019


Ptychographic X-ray nanotomography quantifies mineral distributions in human dentine
text, January 2015


Phase Retrieval with Application to Optical Imaging
preprint, January 2014


Works referencing / citing this record:

X-ray linear dichroic ptychography
dataset, January 2021


X-ray linear dichroic ptychography
dataset, January 2021