DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Cytoprotective metal-organic frameworks for anaerobic bacteria

Abstract

We report a strategy to uniformly wrap Morella thermoacetica bacteria with a metal-organic framework (MOF) monolayer of nanometer thickness for cytoprotection in artificial photosynthesis. The catalytic activity of the MOF enclosure toward decomposition of reactive oxygen species (ROS) reduces the death of strictly anaerobic bacteria by fivefold in the presence of 21% O2, and enables the cytoprotected bacteria to continuously produce acetate from CO2 fixation under oxidative stress. The high definition of the MOF–bacteria interface involving direct bonding between phosphate units on the cell surface and zirconium clusters on MOF monolayer, provides for enhancement of life throughout reproduction. The dynamic nature of the MOF wrapping allows for cell elongation and separation, including spontaneous covering of the newly grown cell surface. Finally, the open-metal sites on the zirconium clusters lead to 600 times more efficient ROS decomposition compared with zirconia nanoparticles.

Authors:
 [1];  [2];  [2];  [3];  [4]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division; Kavli Energy NanoSciences Inst., Berkeley, CA (United States)
  2. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
  3. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division; King Abdulaziz City of Science and Technology, Riyadh (Saudi Arabia)
  4. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division; Univ. of California, Berkeley, CA (United States). Dept. of Materials Science and Engineering; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). fChemical Sciences Division
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Aeronautics and Space Administration (NASA)
OSTI Identifier:
1561896
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 115; Journal Issue: 42; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; cell wrapping; metal-organic frameworks; anaerobic bacteria; artificial photosynthesis; reactive oxygen species

Citation Formats

Ji, Zhe, Zhang, Hao, Liu, Hao, Yaghi, Omar M., and Yang, Peidong. Cytoprotective metal-organic frameworks for anaerobic bacteria. United States: N. p., 2018. Web. doi:10.1073/pnas.1808829115.
Ji, Zhe, Zhang, Hao, Liu, Hao, Yaghi, Omar M., & Yang, Peidong. Cytoprotective metal-organic frameworks for anaerobic bacteria. United States. https://doi.org/10.1073/pnas.1808829115
Ji, Zhe, Zhang, Hao, Liu, Hao, Yaghi, Omar M., and Yang, Peidong. Mon . "Cytoprotective metal-organic frameworks for anaerobic bacteria". United States. https://doi.org/10.1073/pnas.1808829115. https://www.osti.gov/servlets/purl/1561896.
@article{osti_1561896,
title = {Cytoprotective metal-organic frameworks for anaerobic bacteria},
author = {Ji, Zhe and Zhang, Hao and Liu, Hao and Yaghi, Omar M. and Yang, Peidong},
abstractNote = {We report a strategy to uniformly wrap Morella thermoacetica bacteria with a metal-organic framework (MOF) monolayer of nanometer thickness for cytoprotection in artificial photosynthesis. The catalytic activity of the MOF enclosure toward decomposition of reactive oxygen species (ROS) reduces the death of strictly anaerobic bacteria by fivefold in the presence of 21% O2, and enables the cytoprotected bacteria to continuously produce acetate from CO2 fixation under oxidative stress. The high definition of the MOF–bacteria interface involving direct bonding between phosphate units on the cell surface and zirconium clusters on MOF monolayer, provides for enhancement of life throughout reproduction. The dynamic nature of the MOF wrapping allows for cell elongation and separation, including spontaneous covering of the newly grown cell surface. Finally, the open-metal sites on the zirconium clusters lead to 600 times more efficient ROS decomposition compared with zirconia nanoparticles.},
doi = {10.1073/pnas.1808829115},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 42,
volume = 115,
place = {United States},
year = {Mon Oct 01 00:00:00 EDT 2018},
month = {Mon Oct 01 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 111 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Improvement of Biological Organisms Using Functional Material Shells
journal, February 2016

  • Liu, Zhaoming; Xu, Xurong; Tang, Ruikang
  • Advanced Functional Materials, Vol. 26, Issue 12
  • DOI: 10.1002/adfm.201504480

Characterization of Zirconium Phosphate/Polycation Thin Films Grown by Sequential Adsorption Reactions
journal, June 1997

  • Kim, Hyuk-Nyun; Keller, Steven W.; Mallouk, Thomas E.
  • Chemistry of Materials, Vol. 9, Issue 6
  • DOI: 10.1021/cm970027q

Effects of γ-Radiation on Ice 1
journal, July 1956

  • Ghormley, J. A.; Stewart, A. C.
  • Journal of the American Chemical Society, Vol. 78, Issue 13
  • DOI: 10.1021/ja01594a004

Metal-Organic Framework Coatings as Cytoprotective Exoskeletons for Living Cells
journal, July 2016

  • Liang, Kang; Richardson, Joseph J.; Cui, Jiwei
  • Advanced Materials, Vol. 28, Issue 36
  • DOI: 10.1002/adma.201602335

Kinetics, Mechanism, and Activation Energy of H 2 O 2 Decomposition on the Surface of ZrO 2
journal, June 2010

  • Lousada, Cláudio M.; Jonsson, Mats
  • The Journal of Physical Chemistry C, Vol. 114, Issue 25
  • DOI: 10.1021/jp1028933

Nanowire–Bacteria Hybrids for Unassisted Solar Carbon Dioxide Fixation to Value-Added Chemicals
journal, April 2015


Electrostatic Layer-by-Layer Nanoassembly on Biological Microtemplates:  Platelets
journal, May 2002

  • Ai, Hua; Fang, Ming; Jones, Steven A.
  • Biomacromolecules, Vol. 3, Issue 3
  • DOI: 10.1021/bm015659r

Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production
journal, December 2015


Chemical and Fuel Production by Anaerobic Bacteria
journal, October 1980


Biomimetic Encapsulation of Individual Cells with Silica
journal, November 2009

  • Yang, Sung Ho; Lee, Kyung-Bok; Kong, Bokyung
  • Angewandte Chemie International Edition, Vol. 48, Issue 48
  • DOI: 10.1002/anie.200903010

Wall Teichoic Acids of Gram-Positive Bacteria
journal, September 2013


Teichoic Acids and Membrane Function in Bacteria
journal, February 1970

  • Heptinstall, S.; Archibald, A. R.; Baddiley, J.
  • Nature, Vol. 225, Issue 5232
  • DOI: 10.1038/225519a0

Hybrid bioinorganic approach to solar-to-chemical conversion
journal, August 2015

  • Nichols, Eva M.; Gallagher, Joseph J.; Liu, Chong
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 37
  • DOI: 10.1073/pnas.1508075112

Self-Supporting Metal-Organic Layers as Single-Site Solid Catalysts
journal, March 2016

  • Cao, Lingyun; Lin, Zekai; Peng, Fei
  • Angewandte Chemie International Edition, Vol. 55, Issue 16
  • DOI: 10.1002/anie.201512054

Mechanism of H 2 O 2 Decomposition on Transition Metal Oxide Surfaces
journal, April 2012

  • Lousada, Cláudio M.; Johansson, Adam Johannes; Brinck, Tore
  • The Journal of Physical Chemistry C, Vol. 116, Issue 17
  • DOI: 10.1021/jp300255h

Constructing vesicle-based artificial cells with embedded living cells as organelle-like modules
journal, March 2018


Organelle-Specific Triggered Release of Immunostimulatory Oligonucleotides from Intrinsically Coordinated DNA–Metal–Organic Frameworks with Soluble Exoskeleton
journal, October 2017

  • Wang, Zejun; Fu, Yao; Kang, Zhengzhong
  • Journal of the American Chemical Society, Vol. 139, Issue 44
  • DOI: 10.1021/jacs.7b07895

Water splitting–biosynthetic system with CO 2 reduction efficiencies exceeding photosynthesis
journal, June 2016


Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system
journal, February 2015

  • Torella, Joseph P.; Gagliardi, Christopher J.; Chen, Janice S.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1424872112

Chemical diversity in a metal–organic framework revealed by fluorescence lifetime imaging
journal, April 2018


Formation of H 2 O 2 in TiO 2 Photocatalysis of Oxygenated and Deoxygenated Aqueous Systems: A Probe for Photocatalytically Produced Hydroxyl Radicals
journal, May 2014

  • Diesen, Veronica; Jonsson, Mats
  • The Journal of Physical Chemistry C, Vol. 118, Issue 19
  • DOI: 10.1021/jp500315u

Cysteine–Cystine Photoregeneration for Oxygenic Photosynthesis of Acetic Acid from CO 2 by a Tandem Inorganic–Biological Hybrid System
journal, August 2016


An Enzyme-Coated Metal-Organic Framework Shell for Synthetically Adaptive Cell Survival
journal, June 2017

  • Liang, Kang; Richardson, Joseph J.; Doonan, Christian J.
  • Angewandte Chemie International Edition, Vol. 56, Issue 29
  • DOI: 10.1002/anie.201704120

Nanocoating of Single Cells: From Maintenance of Cell Viability to Manipulation of Cellular Activities
journal, January 2014


Biomimetic Encapsulation of Individual Cells with Silica
journal, November 2009

  • Yang, Sung Ho; Lee, Kyung-Bok; Kong, Bokyung
  • Angewandte Chemie, Vol. 121, Issue 48
  • DOI: 10.1002/ange.200903010

An Enzyme-Coated Metal-Organic Framework Shell for Synthetically Adaptive Cell Survival
journal, June 2017

  • Liang, Kang; Richardson, Joseph J.; Doonan, Christian J.
  • Angewandte Chemie, Vol. 129, Issue 29
  • DOI: 10.1002/ange.201704120

Self-Supporting Metal-Organic Layers as Single-Site Solid Catalysts
journal, March 2016


Nanocoating of Single Cells: From Maintenance of Cell Viability to Manipulation of Cellular Activities
journal, January 2014


Metal-Organic Framework Coatings as Cytoprotective Exoskeletons for Living Cells
journal, July 2016

  • Liang, Kang; Richardson, Joseph J.; Cui, Jiwei
  • Advanced Materials, Vol. 28, Issue 36
  • DOI: 10.1002/adma.201602335

Self-Supporting Metal-Organic Layers as Single-Site Solid Catalysts
journal, March 2016

  • Cao, Lingyun; Lin, Zekai; Peng, Fei
  • Angewandte Chemie International Edition, Vol. 55, Issue 16
  • DOI: 10.1002/anie.201512054

An Enzyme-Coated Metal-Organic Framework Shell for Synthetically Adaptive Cell Survival
journal, June 2017

  • Liang, Kang; Richardson, Joseph J.; Doonan, Christian J.
  • Angewandte Chemie International Edition, Vol. 56, Issue 29
  • DOI: 10.1002/anie.201704120

Nanowire–Bacteria Hybrids for Unassisted Solar Carbon Dioxide Fixation to Value-Added Chemicals
journal, April 2015


Electrostatic Layer-by-Layer Nanoassembly on Biological Microtemplates:  Platelets
journal, May 2002

  • Ai, Hua; Fang, Ming; Jones, Steven A.
  • Biomacromolecules, Vol. 3, Issue 3
  • DOI: 10.1021/bm015659r

Effects of γ-Radiation on Ice 1
journal, July 1956

  • Ghormley, J. A.; Stewart, A. C.
  • Journal of the American Chemical Society, Vol. 78, Issue 13
  • DOI: 10.1021/ja01594a004

Organelle-Specific Triggered Release of Immunostimulatory Oligonucleotides from Intrinsically Coordinated DNA–Metal–Organic Frameworks with Soluble Exoskeleton
journal, October 2017

  • Wang, Zejun; Fu, Yao; Kang, Zhengzhong
  • Journal of the American Chemical Society, Vol. 139, Issue 44
  • DOI: 10.1021/jacs.7b07895

Teichoic Acids and Membrane Function in Bacteria
journal, February 1970

  • Heptinstall, S.; Archibald, A. R.; Baddiley, J.
  • Nature, Vol. 225, Issue 5232
  • DOI: 10.1038/225519a0

Chemical diversity in a metal–organic framework revealed by fluorescence lifetime imaging
journal, April 2018


Constructing vesicle-based artificial cells with embedded living cells as organelle-like modules
journal, March 2018


Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system
journal, February 2015

  • Torella, Joseph P.; Gagliardi, Christopher J.; Chen, Janice S.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 8
  • DOI: 10.1073/pnas.1424872112

Hybrid bioinorganic approach to solar-to-chemical conversion
journal, August 2015

  • Nichols, Eva M.; Gallagher, Joseph J.; Liu, Chong
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 37
  • DOI: 10.1073/pnas.1508075112

Tolerance and Metabolic Response of Acetogenic Bacteria toward Oxygen
journal, February 2002


Hydrogen-Dependent Oxygen Reduction by Homoacetogenic Bacteria Isolated from Termite Guts
journal, February 2003


Cytochrome bd Oxidase, Oxidative Stress, and Dioxygen Tolerance of the Strictly Anaerobic Bacterium Moorella thermoacetica
journal, March 2005


Wall Teichoic Acids of Gram-Positive Bacteria
journal, September 2013


Chemical and Fuel Production by Anaerobic Bacteria
journal, October 1980


Works referencing / citing this record:

Biocatalytic Metal‐Organic Framework‐Based Artificial Cells
journal, August 2019

  • Liu, Jian; Guo, Ziyi; Liang, Kang
  • Advanced Functional Materials, Vol. 29, Issue 45
  • DOI: 10.1002/adfm.201905321

SupraCells: Living Mammalian Cells Protected within Functional Modular Nanoparticle‐Based Exoskeletons
journal, April 2019


Nanoarchitectonics of Biofunctionalized Metal–Organic Frameworks with Biological Macromolecules and Living Cells
journal, May 2019


Photoluminescent organisms: how to make fungi glow through biointegration with lanthanide metal-organic frameworks
journal, May 2019


Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids
journal, January 2019

  • Cestellos-Blanco, Stefano; Zhang, Hao; Yang, Peidong
  • Faraday Discussions, Vol. 215
  • DOI: 10.1039/c8fd00187a

Effective loading of cisplatin into a nanoscale UiO-66 metal–organic framework with preformed defects
journal, January 2019

  • Lin, Shi-Xin; Pan, Wei-Lun; Niu, Ru-Jie
  • Dalton Transactions, Vol. 48, Issue 16
  • DOI: 10.1039/c9dt00719a

Cisplatin delivery, anticancer and antibacterial properties of Fe/SBA-16/ZIF-8 nanocomposite
journal, January 2019

  • Balasamy, Rabindran Jermy; Ravinayagam, Vijaya; Alomari, Munther
  • RSC Advances, Vol. 9, Issue 72
  • DOI: 10.1039/c9ra07461a

Photoluminescent organisms: how to make fungi glow through biointegration with lanthanide metal-organic frameworks
journal, May 2019


Nanobiohybrids: Materials approaches for bioaugmentation
journal, March 2020


Metal-Organic Framework Nanoparticle-Based Biomineralization: A New Strategy toward Cancer Treatment
journal, January 2019

  • Chu, Chengchao; Su, Min; Zhu, Jing
  • Theranostics, Vol. 9, Issue 11
  • DOI: 10.7150/thno.33539