Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting in Archaeoglobus fulgidus Cells
Abstract
Inorganic storage granules have long been recognized in bacterial and eukaryotic cells but were only recently identified in archaeal cells. Here, we report the cellular organization and chemical compositions of storage granules in the Euryarchaeon, Archaeoglobus fulgidusstrain VC16, a hyperthermophilic, anaerobic, and sulfate-reducing microorganism. Dense granules were apparent inA. fulgiduscells imaged by cryo electron microscopy (cryoEM) but not so by negative stain electron microscopy. Cryo electron tomography (cryoET) revealed that each cell contains one to several dense granules located near the cell membrane. Energy dispersive X-ray (EDX) spectroscopy and scanning transmission electron microscopy (STEM) show that, surprisingly, each cell contains not just one but often two types of granules with different elemental compositions. One type, named iron sulfide body (ISB), is composed mainly of the elements iron and sulfur plus copper; and the other one, called polyphosphate body (PPB), is composed of phosphorus and oxygen plus magnesium, calcium, and aluminum. PPBs are likely used for energy storage and/or metal sequestration/detoxification. ISBs could result from the reduction of sulfate to sulfide via anaerobic energy harvesting pathways and may be associated with energy and/or metal storage or detoxification. The exceptional ability of these archaeal cells to sequester different elements may have novelmore »
- Authors:
-
- Department of Microbiology, Immunology, and Molecular Genetics, UCLA, Los Angeles, CA 90095, USA; Electron Imaging Center for Nanomachines, California NanoSystems Institute, UCLA, Los Angeles, CA 90095, USA; The UCLA Biomedical Engineering Interdepartmental Program, UCLA, Los Angeles, CA 09905, USA
- Department of Microbiology, Immunology, and Molecular Genetics, UCLA, Los Angeles, CA 90095, USA; Institute of Industrial Biotechnology, GC University, Lahore 54000, Pakistan
- Department of Microbiology, Immunology, and Molecular Genetics, UCLA, Los Angeles, CA 90095, USA
- Department of Microbiology, Immunology, and Molecular Genetics, UCLA, Los Angeles, CA 90095, USA; The UCLA-DOE Institute of Genomics and Proteomics, UCLA, Los Angeles, CA 90095, USA
- Publication Date:
- Research Org.:
- Univ. of California, Los Angeles, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1248066
- Alternate Identifier(s):
- OSTI ID: 1258738
- Grant/Contract Number:
- FC02-02ER63421; FG03-86ER13498
- Resource Type:
- Published Article
- Journal Name:
- Archaea
- Additional Journal Information:
- Journal Name: Archaea Journal Volume: 2016; Journal ID: ISSN 1472-3646
- Publisher:
- Hindawi
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES
Citation Formats
Toso, Daniel B., Javed, Muhammad Mohsin, Czornyj, Elizabeth, Gunsalus, Robert P., and Zhou, Z. Hong. Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting in Archaeoglobus fulgidus Cells. United States: N. p., 2016.
Web. doi:10.1155/2016/4706532.
Toso, Daniel B., Javed, Muhammad Mohsin, Czornyj, Elizabeth, Gunsalus, Robert P., & Zhou, Z. Hong. Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting in Archaeoglobus fulgidus Cells. United States. https://doi.org/10.1155/2016/4706532
Toso, Daniel B., Javed, Muhammad Mohsin, Czornyj, Elizabeth, Gunsalus, Robert P., and Zhou, Z. Hong. Fri .
"Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting in Archaeoglobus fulgidus Cells". United States. https://doi.org/10.1155/2016/4706532.
@article{osti_1248066,
title = {Discovery and Characterization of Iron Sulfide and Polyphosphate Bodies Coexisting in Archaeoglobus fulgidus Cells},
author = {Toso, Daniel B. and Javed, Muhammad Mohsin and Czornyj, Elizabeth and Gunsalus, Robert P. and Zhou, Z. Hong},
abstractNote = {Inorganic storage granules have long been recognized in bacterial and eukaryotic cells but were only recently identified in archaeal cells. Here, we report the cellular organization and chemical compositions of storage granules in the Euryarchaeon, Archaeoglobus fulgidusstrain VC16, a hyperthermophilic, anaerobic, and sulfate-reducing microorganism. Dense granules were apparent inA. fulgiduscells imaged by cryo electron microscopy (cryoEM) but not so by negative stain electron microscopy. Cryo electron tomography (cryoET) revealed that each cell contains one to several dense granules located near the cell membrane. Energy dispersive X-ray (EDX) spectroscopy and scanning transmission electron microscopy (STEM) show that, surprisingly, each cell contains not just one but often two types of granules with different elemental compositions. One type, named iron sulfide body (ISB), is composed mainly of the elements iron and sulfur plus copper; and the other one, called polyphosphate body (PPB), is composed of phosphorus and oxygen plus magnesium, calcium, and aluminum. PPBs are likely used for energy storage and/or metal sequestration/detoxification. ISBs could result from the reduction of sulfate to sulfide via anaerobic energy harvesting pathways and may be associated with energy and/or metal storage or detoxification. The exceptional ability of these archaeal cells to sequester different elements may have novel bioengineering applications.},
doi = {10.1155/2016/4706532},
journal = {Archaea},
number = ,
volume = 2016,
place = {United States},
year = {Fri Jan 01 00:00:00 EST 2016},
month = {Fri Jan 01 00:00:00 EST 2016}
}
https://doi.org/10.1155/2016/4706532
Web of Science
Works referenced in this record:
Heat Shock Response of Archaeoglobus fulgidus
journal, August 2005
- Rohlin, L.; Trent, J. D.; Salmon, K.
- Journal of Bacteriology, Vol. 187, Issue 17
Characterization of a New Type of Dissimilatory Sulfite Reductase Present in Thermodesulfobacterium commune
journal, January 1983
- Hatchikian, E. C.; Zeikus, J. G.
- Journal of Bacteriology, Vol. 153, Issue 3
Polyphosphate and Phosphate Pump
journal, October 2000
- Kulaev, I.; Kulakovskaya, T.
- Annual Review of Microbiology, Vol. 54, Issue 1
Ultrastructural investigation of 12 Methanosarcinae and related species grown on methanol for occurrence of polyphosphatelike inclusions
journal, September 1983
- Scherer, P. A.; Bochem, H. -P.
- Canadian Journal of Microbiology, Vol. 29, Issue 9
Disclosure of the mycobacterial outer membrane: Cryo-electron tomography and vitreous sections reveal the lipid bilayer structure
journal, March 2008
- Hoffmann, C.; Leis, A.; Niederweis, M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 10
Effect of growth temperature on ether lipid biochemistry in Archaeoglobus fulgidus
journal, December 2007
- Lai, Denton; Springstead, James R.; Monbouquette, Harold G.
- Extremophiles, Vol. 12, Issue 2
From invagination to navigation: The story of magnetosome-associated proteins in magnetotactic bacteria: Magnetosome Proteins in Magnetotactic Bacteria
journal, November 2015
- Barber-Zucker, Shiran; Keren-Khadmy, Noa; Zarivach, Raz
- Protein Science, Vol. 25, Issue 2
Volcanoes, Fluids, and Life at Mid-Ocean Ridge Spreading Centers
journal, May 2002
- Kelley, Deborah S.; Baross, John A.; Delaney, John R.
- Annual Review of Earth and Planetary Sciences, Vol. 30, Issue 1
Controlled Biomineralization of Magnetite (Fe(inf3)O(inf4)) and Greigite (Fe(inf3)S(inf4)) in a Magnetotactic Bacterium.
journal, January 1995
- Bazylinski, D. A.; Frankel, R. B.; Heywood, B. R.
- Applied and environmental microbiology, Vol. 61, Issue 9
New aspects of inorganic polyphosphate metabolism and function
journal, January 1999
- Kulaev, Igor; Vagabov, Vladimir; Kulakovskaya, Tatiana
- Journal of Bioscience and Bioengineering, Vol. 88, Issue 2
Archaeoglobus fulgidus Isolated from Hot North Sea Oil Field Waters
journal, January 1994
- Beeder, Janiche; Nilsen, Roald Kåre; Rosnes, Jan Thomas
- Applied and Environmental Microbiology, Vol. 60, Issue 4
Formation of thiosulfate and trithionate during sulfite reduction by washed cells of Desulfovibrio desulfuricans
journal, September 1990
- Fitz, Robert M.; Cypionka, Heribert
- Archives of Microbiology, Vol. 154, Issue 4
Inorganic Polyphosphate: A Molecule of Many Functions
journal, June 1999
- Kornberg, Arthur; Rao, Narayana N.; Ault-Riché, Dana
- Annual Review of Biochemistry, Vol. 68, Issue 1
Role of the S layer in morphogenesis and cell division of the archaebacterium Methanocorpusculum sinense.
journal, November 1991
- Pum, D.; Messner, P.; Sleytr, U. B.
- Journal of Bacteriology, Vol. 173, Issue 21
Three-dimensional Reconstruction of the Surface Protein of the Extremely Thermophilic Archaebacterium Archaeoglobus fulgidus
journal, August 1990
- Kessel, Martin; Volker, Susanne; Santarius, Ute
- Systematic and Applied Microbiology, Vol. 13, Issue 3
Inorganic Polyphosphate: Essential for Growth and Survival
journal, June 2009
- Rao, Narayana N.; Gómez-García, María R.; Kornberg, Arthur
- Annual Review of Biochemistry, Vol. 78, Issue 1
The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus
journal, November 1997
- Klenk, Hans-Peter; Clayton, Rebecca A.; Tomb, Jean-Francois
- Nature, Vol. 390, Issue 6658
Structural, mass and elemental analyses of storage granules in methanogenic archaeal cells: Storage granules in methanogenic archaeal cells
journal, August 2011
- Toso, Daniel B.; Henstra, Anne M.; Gunsalus, Robert P.
- Environmental Microbiology, Vol. 13, Issue 9
Elemental characterization of microorganism granules by EFTEM in the tube wall of a deep-sea vent invertebrate
journal, September 2002
- Lechaire, Jean-Pierre; Shillito, Bruce; Frébourg, Ghislaine
- Biology of the Cell, Vol. 94, Issue 4-5
Computer Visualization of Three-Dimensional Image Data Using IMOD
journal, January 1996
- Kremer, James R.; Mastronarde, David N.; McIntosh, J. Richard
- Journal of Structural Biology, Vol. 116, Issue 1
Formation of Thiosulfate from Sulfite by Desulfovibrio vulgaris
journal, January 1969
- Suh, Byungse; Akagi, J. M.
- Journal of Bacteriology, Vol. 99, Issue 1
Archaeoglobus fulgidus gen. nov., sp. nov.: a New Taxon of Extremely Thermophilic Archaebacteria
journal, March 1988
- Stetter, Karl O.
- Systematic and Applied Microbiology, Vol. 10, Issue 2
Hyperthermophilic archaea are thriving in deep North Sea and Alaskan oil reservoirs
journal, October 1993
- Stetter, K. O.; Huber, R.; Blöchl, E.
- Nature, Vol. 365, Issue 6448
Copper tolerance of the thermoacidophilic archaeon Sulfolobus metallicus: possible role of polyphosphate metabolism
journal, January 2006
- Remonsellez, Francisco; Orell, Alvaro Orell; Jerez, Carlos A. Jerez
- Microbiology, Vol. 152, Issue 1, p. 59-66
Isolation of Extremely Thermophilic Sulfate Reducers: Evidence for a Novel Branch of Archaebacteria
journal, May 1987
- Stetter, K. O.; Lauerer, G.; Thomm, M.
- Science, Vol. 236, Issue 4803
[25] Biofilm formation in hyperthermophilic archaea
book, January 1999
- Hartzell, Patricia L.; Millstein, Jack; LaPaglia, Christopher
- Biofilms