Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy
Abstract
Phylogenetically diverse environmental ANME archaea and sulfate-reducing bacteria cooperatively catalyze the anaerobic oxidation of methane oxidation (AOM) in multicelled consortia within methane seep environments. To better understand these cells and their symbiotic associations, we applied a suite of electron microscopy approaches, including correlative fluorescence in situ hybridization-electron microscopy (FISH-EM), transmission electron microscopy (TEM), and serial block face scanning electron microscopy (SBEM) three-dimensional (3D) reconstructions. FISH-EM of methane seep-derived consortia revealed phylogenetic variability in terms of cell morphology, ultrastructure, and storage granules. Representatives of the ANME-2b clade, but not other ANME-2 groups, contained polyphosphate-like granules, while some bacteria associated with ANME-2a/2c contained two distinct phases of iron mineral chains resembling magnetosomes. 3D segmentation of two ANME-2 consortium types revealed cellular volumes of ANME and their symbiotic partners that were larger than previous estimates based on light microscopy. Polyphosphate-like granule-containing ANME (tentatively termed ANME-2b) were larger than both ANME with no granules and partner bacteria. This cell type was observed with up to 4 granules per cell, and the volume of the cell was larger in proportion to the number of granules inside it, but the percentage of the cell occupied by these granules did not vary with granule number. Here, thesemore »
- Authors:
-
[1];
- California Inst. of Technology (CalTech), Pasadena, CA (United States); EN Center for Sustainable Resource Science (CSRS), Saitama (Japan); Tokyo Institute of Technology, Tokyo (Japan)
- California Inst. of Technology (CalTech), Pasadena, CA (United States)
- Univ. of California, San Diego (UCSD), La Jolla, CA (United States)
- Univ. of California, San Diego (UCSD), La Jolla, CA (United States); Salk Institute for Biological Sciences, La Jolla, CA (United States); HHMI Janelia Research Campus, Ashburn, VA (United States)
- Kyoto Univ., Kyoto (Japan)
- Publication Date:
- Research Org.:
- California Institute of Technology (CalTech), Pasadena, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1529227
- Grant/Contract Number:
- SC0004949
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 84; Journal Issue: 11; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ANME; DIET; polyphosphate metabolism; anaerobic methane oxidation; electron microscopy; fluorescence image analysis; sulfate reduction; syntrophy; ultrastructure
Citation Formats
McGlynn, Shawn E., Chadwick, Grayson L., O'Neill, Ariel, Mackey, Mason, Thor, Andrea, Deerinck, Thomas J., Ellisman, Mark H., Orphan, Victoria J., and Atomi, Haruyuki. Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. United States: N. p., 2018.
Web. doi:10.1128/aem.00399-18.
McGlynn, Shawn E., Chadwick, Grayson L., O'Neill, Ariel, Mackey, Mason, Thor, Andrea, Deerinck, Thomas J., Ellisman, Mark H., Orphan, Victoria J., & Atomi, Haruyuki. Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy. United States. https://doi.org/10.1128/aem.00399-18
McGlynn, Shawn E., Chadwick, Grayson L., O'Neill, Ariel, Mackey, Mason, Thor, Andrea, Deerinck, Thomas J., Ellisman, Mark H., Orphan, Victoria J., and Atomi, Haruyuki. Fri .
"Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy". United States. https://doi.org/10.1128/aem.00399-18. https://www.osti.gov/servlets/purl/1529227.
@article{osti_1529227,
title = {Subgroup Characteristics of Marine Methane-Oxidizing ANME-2 Archaea and Their Syntrophic Partners as Revealed by Integrated Multimodal Analytical Microscopy},
author = {McGlynn, Shawn E. and Chadwick, Grayson L. and O'Neill, Ariel and Mackey, Mason and Thor, Andrea and Deerinck, Thomas J. and Ellisman, Mark H. and Orphan, Victoria J. and Atomi, Haruyuki},
abstractNote = {Phylogenetically diverse environmental ANME archaea and sulfate-reducing bacteria cooperatively catalyze the anaerobic oxidation of methane oxidation (AOM) in multicelled consortia within methane seep environments. To better understand these cells and their symbiotic associations, we applied a suite of electron microscopy approaches, including correlative fluorescence in situ hybridization-electron microscopy (FISH-EM), transmission electron microscopy (TEM), and serial block face scanning electron microscopy (SBEM) three-dimensional (3D) reconstructions. FISH-EM of methane seep-derived consortia revealed phylogenetic variability in terms of cell morphology, ultrastructure, and storage granules. Representatives of the ANME-2b clade, but not other ANME-2 groups, contained polyphosphate-like granules, while some bacteria associated with ANME-2a/2c contained two distinct phases of iron mineral chains resembling magnetosomes. 3D segmentation of two ANME-2 consortium types revealed cellular volumes of ANME and their symbiotic partners that were larger than previous estimates based on light microscopy. Polyphosphate-like granule-containing ANME (tentatively termed ANME-2b) were larger than both ANME with no granules and partner bacteria. This cell type was observed with up to 4 granules per cell, and the volume of the cell was larger in proportion to the number of granules inside it, but the percentage of the cell occupied by these granules did not vary with granule number. Here, these results illuminate distinctions between ANME-2 archaeal lineages and partnering bacterial populations that are apparently unified in their ability to perform anaerobic methane oxidation.},
doi = {10.1128/aem.00399-18},
journal = {Applied and Environmental Microbiology},
number = 11,
volume = 84,
place = {United States},
year = {2018},
month = {4}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 17 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Automated tilt series alignment and tomographic reconstruction in IMOD
journal, February 2017
- Mastronarde, David N.; Held, Susannah R.
- Journal of Structural Biology, Vol. 197, Issue 2
Mixed-Valence Cytoplasmic Iron Granules Are Linked to Anaerobic Respiration
journal, December 2006
- Glasauer, S.; Langley, S.; Boyanov, M.
- Applied and Environmental Microbiology, Vol. 73, Issue 3
A single-cell view on the ecophysiology of anaerobic phototrophic bacteria
journal, November 2008
- Musat, N.; Halm, H.; Winterholler, B.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 46
The H + -pyrophosphatase of Rhodospirillum rubrum Is Predominantly Located in Polyphosphate-rich Acidocalcisomes
journal, September 2004
- Seufferheld, Manfredo; Lea, Christopher R.; Vieira, Mauricio
- Journal of Biological Chemistry, Vol. 279, Issue 49
Microbial Reefs in the Black Sea Fueled by Anaerobic Oxidation of Methane
journal, August 2002
- Michaelis, W.
- Science, Vol. 297, Issue 5583
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
PPK1 and PPK2 — which polyphosphate kinase is older?
journal, January 2014
- Achbergerová, Lucia; Nahálka, Jozef
- Biologia, Vol. 69, Issue 3
In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulfate
journal, January 2007
- Nauhaus, Katja; Albrecht, Melanie; Elvert, Marcus
- Environmental Microbiology, Vol. 9, Issue 1
Pre-embedding immunolabeling for electron microscopy: An evaluation of permeabilization methods and markers
journal, July 1998
- Humbel, Bruno M.; de Jong, Margo D. M.; Müller, Wally H.
- Microscopy Research and Technique, Vol. 42, Issue 1
Relationships between Biovolume and Biomass of Naturally Derived Marine Bacterioplankton †
journal, January 1987
- Lee, Sanghoon; Fuhrman, Jed A.
- Applied and Environmental Microbiology, Vol. 53, Issue 6
Candidatus Desulfofervidus auxilii, a hydrogenotrophic sulfate-reducing bacterium involved in the thermophilic anaerobic oxidation of methane : The partner bacterium in thermophilic methanotrophy
journal, April 2016
- Krukenberg, Viola; Harding, Katie; Richter, Michael
- Environmental Microbiology, Vol. 18, Issue 9
Extracellular electron transfer: wires, capacitors, iron lungs, and more
journal, June 2008
- Lovley, Derek R.
- Geobiology, Vol. 6, Issue 3
Bacterial Intracellular Sulfur Globules: Structure and Function
journal, January 2013
- Maki, James S.
- Journal of Molecular Microbiology and Biotechnology, Vol. 23, Issue 4-5
A polyphosphate kinase (PPK2) widely conserved in bacteria
journal, December 2002
- Zhang, H.; Ishige, K.; Kornberg, A.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 26
Bacterioplankton Compositions of Lakes and Oceans: a First Comparison Based on Fluorescence In Situ Hybridization
journal, August 1999
- Glöckner, Frank Oliver; Fuchs, Bernhard M.; Amann, Rudolf
- Applied and Environmental Microbiology, Vol. 65, Issue 8
Patterns of 15 N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS
journal, July 2009
- Orphan, Victoria J.; Turk, Kendra A.; Green, Abigail M.
- Environmental Microbiology, Vol. 11, Issue 7
Life Cycles in the Methanogenic Archaebacterium Methanosarcina mazei†
journal, January 1986
- Robinson, Ralph W.
- Applied and Environmental Microbiology, Vol. 52, Issue 1
Double Labeling of Oligonucleotide Probes for Fluorescence In Situ Hybridization (DOPE-FISH) Improves Signal Intensity and Increases rRNA Accessibility
journal, December 2009
- Stoecker, K.; Dorninger, C.; Daims, H.
- Applied and Environmental Microbiology, Vol. 76, Issue 3
Insights into the genomes of archaea mediating the anaerobic oxidation of methane: Genomes of methanotrophic archaea
journal, July 2005
- Meyerdierks, Anke; Kube, Michael; Lombardot, Thierry
- Environmental Microbiology, Vol. 7, Issue 12
High-performance serial block-face SEM of nonconductive biological samples enabled by focal gas injection-based charge compensation: HIGH-PERFORMANCE SERIAL BLOCK-FACE SEM
journal, December 2017
- Deerinck, T. J.; Shone, T. M.; Bushong, E. A.
- Journal of Microscopy, Vol. 270, Issue 2
Magnetotactic Bacteria
journal, October 1982
- Blakemore, R. P.
- Annual Review of Microbiology, Vol. 36, Issue 1
Fe304 and Fe3S4 in a bacterium
journal, November 1993
- Bazylizinki, Dennis A.; Heywood, Brigid R.; Mann, Stephen
- Nature, Vol. 366, Issue 6452
Magnetic Guidance of Organisms
journal, June 1984
- Frankel, R. B.
- Annual Review of Biophysics and Bioengineering, Vol. 13, Issue 1
Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments
journal, May 2002
- Orphan, V. J.; House, C. H.; Hinrichs, K.-U.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 11, p. 7663-7668
Abundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides
journal, January 1998
- Manz, Werner; Eisenbrecher, Michael; Neu, Thomas R.
- FEMS Microbiology Ecology, Vol. 25, Issue 1
Anaerobic methane oxidation by archaea/sulfate-reducing bacteria aggregates: 1. Thermodynamic and physical constraints
journal, December 2009
- Alperin, M. J.; Hoehler, T. M.
- American Journal of Science, Vol. 309, Issue 10
Energy-dispersive X-ray microanalysis of the methanogenMethanosarcina barkeri ‘Fusaro’ grown on methanol and in the presence of heavy metals
journal, July 1983
- Scherer, Paul A.; Bochem, Hans-P
- Current Microbiology, Vol. 9, Issue 4
Single cell activity reveals direct electron transfer in methanotrophic consortia
journal, September 2015
- McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P.
- Nature, Vol. 526, Issue 7574
Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions
journal, January 2008
- Orcutt, B.; Meile, C.
- Biogeosciences, Vol. 5, Issue 6
The identification and biogeochemical interpretation of fossil magnetotactic bacteria
journal, January 2008
- Kopp, Robert E.; Kirschvink, Joseph L.
- Earth-Science Reviews, Vol. 86, Issue 1-4
A Metagenomics-Based Metabolic Model of Nitrate-Dependent Anaerobic Oxidation of Methane by Methanoperedens-Like Archaea
journal, December 2015
- Arshad, Arslan; Speth, Daan R.; de Graaf, Rob M.
- Frontiers in Microbiology, Vol. 6
Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics
journal, September 2004
- Hallam, S. J.
- Science, Vol. 305, Issue 5689
Methane-derived carbonate build-ups and associated microbial communities at cold seeps on the lower Crimean shelf (Black Sea)
journal, July 2005
- Reitner, Joachim; Peckmann, Jörn; Reimer, Andreas
- Facies, Vol. 51, Issue 1-4
Immunological detection of enzymes for sulfate reduction in anaerobic methane-oxidizing consortia: Localization of enzymes for sulfate reduction
journal, October 2012
- Milucka, Jana; Widdel, Friedrich; Shima, Seigo
- Environmental Microbiology, Vol. 15, Issue 5
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia
journal, June 2016
- Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 28
Metabolic Capabilities of Microorganisms Involved in and Associated with the Anaerobic Oxidation of Methane
journal, February 2016
- Wegener, Gunter; Krukenberg, Viola; Ruff, S. Emil
- Frontiers in Microbiology, Vol. 7
Role of Inorganic Polyphosphate in Promoting Ribosomal Protein Degradation by the Lon Protease in E. coli
journal, July 2001
- Kuroda, A.
- Science, Vol. 293, Issue 5530
Mapping the Speciation of Iron in Pseudomonas aeruginosa Biofilms Using Scanning Transmission X-ray Microscopy
journal, December 2008
- Hunter, Ryan C.; Hitchcock, Adam P.; Dynes, James J.
- Environmental Science & Technology, Vol. 42, Issue 23
Community Composition and Ultrastructure of a Nitrate-Dependent Anaerobic Methane-Oxidizing Enrichment Culture
journal, November 2017
- Gambelli, Lavinia; Guerrero-Cruz, Simon; Mesman, Rob J.
- Applied and Environmental Microbiology, Vol. 84, Issue 3
Development of 16S rRNA gene-targeted primers for detection of archaeal anaerobic methanotrophs (ANMEs)
journal, August 2009
- Miyashita, Ai; Mochimaru, Hanako; Kazama, Hiromi
- FEMS Microbiology Letters, Vol. 297, Issue 1
Developing 3D SEM in a broad biological context: 3D SEM
journal, January 2015
- Kremer, A.; Lippens, S.; Bartunkova, S.
- Journal of Microscopy, Vol. 259, Issue 2
Magnetotactic Bacteria and Magnetosomes
journal, November 2008
- Faivre, Damien; Schüler, Dirk
- Chemical Reviews, Vol. 108, Issue 11
Sulfur vesicles from Thermococcales: A possible role in sulfur detoxifying mechanisms
journal, November 2015
- Gorlas, A.; Marguet, E.; Gill, S.
- Biochimie, Vol. 118
Dual-Axis Tomography: An Approach with Alignment Methods That Preserve Resolution
journal, December 1997
- Mastronarde, David N.
- Journal of Structural Biology, Vol. 120, Issue 3
In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area
journal, May 2002
- Nauhaus, Katja; Boetius, Antje; Kruger, Martin
- Environmental Microbiology, Vol. 4, Issue 5
A Cultured Greigite-Producing Magnetotactic Bacterium in a Novel Group of Sulfate-Reducing Bacteria
journal, December 2011
- Lefevre, C. T.; Menguy, N.; Abreu, F.
- Science, Vol. 334, Issue 6063
ppGpp and Polyphosphate Modulate Cell Cycle Progression in Caulobacter crescentus
journal, October 2011
- Boutte, C. C.; Henry, J. T.; Crosson, S.
- Journal of Bacteriology, Vol. 194, Issue 1
Diversity and Distribution of Methanotrophic Archaea at Cold Seeps
journal, January 2005
- Knittel, K.; Losekann, T.; Boetius, A.
- Applied and Environmental Microbiology, Vol. 71, Issue 1
Direct Image-Based Correlative Microscopy Technique for Coupling Identification and Structural Investigation of Bacterial Symbionts Associated with Metazoans
journal, April 2011
- Halary, Sébastien; Duperron, Sébastien; Boudier, Thomas
- Applied and Environmental Microbiology, Vol. 77, Issue 12
Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage
journal, July 2013
- Haroon, Mohamed F.; Hu, Shihu; Shi, Ying
- Nature, Vol. 500, Issue 7464
Concretionary methane-seep carbonates and associated microbial communities in Black Sea sediments
journal, October 2005
- Reitner, J.; Peckmann, J.; Blumenberg, M.
- Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 227, Issue 1-3
Shedding light on cell compartmentation in the candidate phylum Poribacteria by high resolution visualisation and transcriptional profiling
journal, October 2016
- Jahn, Martin T.; Markert, Sebastian M.; Ryu, Taewoo
- Scientific Reports, Vol. 6, Issue 1
Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon
journal, October 2008
- Comolli, Luis R.; Baker, Brett J.; Downing, Kenneth H.
- The ISME Journal, Vol. 3, Issue 2
S-layers at second glance? Altiarchaeal grappling hooks (hami) resemble archaeal S-layer proteins in structure and sequence
journal, June 2015
- Perras, Alexandra K.; Daum, Bertram; Ziegler, Christine
- Frontiers in Microbiology, Vol. 6
Cell organization and ultrastructure of a magnetotactic multicellular organism
journal, March 2004
- Keim, Carolina N.; Abreu, Fernanda; Lins, Ulysses
- Journal of Structural Biology, Vol. 145, Issue 3
Comparative Analysis of Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in Anoxic Marine Sediments
journal, April 2001
- Orphan, V. J.; Hinrichs, K. -U.; Ussler, W.
- Applied and Environmental Microbiology, Vol. 67, Issue 4
Correlative microscopy for phylogenetic and ultrastructural characterization of microbial communities: Correlative TEM and CARD-FISH imaging
journal, August 2011
- Knierim, Bernhard; Luef, Birgit; Wilmes, Paul
- Environmental Microbiology Reports, Vol. 4, Issue 1
Diverse syntrophic partnerships from deep-sea methane vents revealed by direct cell capture and metagenomics
journal, May 2008
- Pernthaler, A.; Dekas, A. E.; Brown, C. T.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 19
Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment
journal, October 2002
- Loy, A.; Lehner, A.; Lee, N.
- Applied and Environmental Microbiology, Vol. 68, Issue 10
Linking Ultrastructure and Function in Four Genera of Anaerobic Ammonium-Oxidizing Bacteria: Cell Plan, Glycogen Storage, and Localization of Cytochrome c Proteins
journal, November 2007
- van Niftrik, L.; Geerts, W. J. C.; van Donselaar, E. G.
- Journal of Bacteriology, Vol. 190, Issue 2
A new view of the tree of life
journal, April 2016
- Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik
- Nature Microbiology, Vol. 1, Issue 5
A marine microbial consortium apparently mediating anaerobic oxidation of methane
journal, October 2000
- Boetius, Antje; Ravenschlag, Katrin; Schubert, Carsten J.
- Nature, Vol. 407, Issue 6804
Metagenome and mRNA expression analyses of anaerobic methanotrophic archaea of the ANME-1 group
journal, February 2010
- Meyerdierks, Anke; Kube, Michael; Kostadinov, Ivaylo
- Environmental Microbiology, Vol. 12, Issue 2
Detection of Metabolic Key Enzymes of Methane Turnover Processes in Cold Seep Microbial Biofilms
journal, January 2013
- Wrede, Christoph; Krukenberg, Viola; Dreier, Anne
- Geomicrobiology Journal, Vol. 30, Issue 3
Bioenergetics and anaerobic respiratory chains of aceticlastic methanogens
journal, July 2014
- Welte, Cornelia; Deppenmeier, Uwe
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
Polyphosphate granule biogenesis is temporally and functionally tied to cell cycle exit during starvation in Pseudomonas aeruginosa
journal, March 2017
- Racki, Lisa R.; Tocheva, Elitza I.; Dieterle, Michael G.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 12
Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008
- Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
- Nature Reviews Microbiology, Vol. 6, Issue 8
Dominant Microbial Populations in Limestone-Corroding Stream Biofilms, Frasassi Cave System, Italy
journal, August 2006
- Macalady, J. L.; Lyon, E. H.; Koffman, B.
- Applied and Environmental Microbiology, Vol. 72, Issue 8
Fluorescence in situ hybridisation coupled to ultra small immunogold detection to identify prokaryotic cells using transmission and scanning electron microscopy
journal, October 2005
- Gérard, Emmanuelle; Guyot, François; Philippot, Pascal
- Journal of Microbiological Methods, Vol. 63, Issue 1
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life
journal, September 2017
- Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria
- Nature Microbiology, Vol. 2, Issue 11
Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia
journal, October 2009
- Dekas, A. E.; Poretsky, R. S.; Orphan, V. J.
- Science, Vol. 326, Issue 5951
The unique structure of archaeal ‘hami’, highly complex cell appendages with nano-grappling hooks: Unique structure of archaeal ‘hami’
journal, March 2005
- Moissl, Christine; Rachel, Reinhard; Briegel, Ariane
- Molecular Microbiology, Vol. 56, Issue 2
Zero-valent sulphur is a key intermediate in marine methane oxidation
journal, November 2012
- Milucka, Jana; Ferdelman, Timothy G.; Polerecky, Lubos
- Nature, Vol. 491, Issue 7425
Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria
journal, October 2015
- Wegener, Gunter; Krukenberg, Viola; Riedel, Dietmar
- Nature, Vol. 526, Issue 7574
Energy Metabolism during Anaerobic Methane Oxidation in ANME Archaea
journal, January 2017
- McGlynn, Shawn E.
- Microbes and environments, Vol. 32, Issue 1
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
Deposition of Biogenic Iron Minerals in a Methane Oxidizing Microbial Mat
journal, January 2013
- Wrede, Christoph; Kokoschka, Sebastian; Dreier, Anne
- Archaea, Vol. 2013
High resolution three-dimensional reconstruction of fibrotic skeletal muscle extracellular matrix: Fibrotic muscle ECM organization
journal, December 2016
- Gillies, Allison R.; Chapman, Mark A.; Bushong, Eric A.
- The Journal of Physiology, Vol. 595, Issue 4
Enhancing Serial Block-Face Scanning Electron Microscopy to Enable High Resolution 3-D Nanohistology of Cells and Tissues
journal, July 2010
- Deerinck, Tj; Bushong, Ea; Lev-Ram, V.
- Microscopy and Microanalysis, Vol. 16, Issue S2
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
Immunological Localization of Coenzyme M Reductase in Anaerobic Methane-Oxidizing Archaea of ANME 1 and ANME 2 Type
journal, June 2008
- Heller, Christina; Hoppert, Michael; Reitner, Joachim
- Geomicrobiology Journal, Vol. 25, Issue 3-4
Methanotrophic archaea possessing diverging methane-oxidizing and electron-transporting pathways
journal, December 2013
- Wang, Feng-Ping; Zhang, Yu; Chen, Ying
- The ISME Journal, Vol. 8, Issue 5
Ultrastructure of ellipsoidal magnetotactic multicellular prokaryotes depicts their complex assemblage and cellular polarity in the context of magnetotaxis: Ultrastructure and magnetotaxis in ellipsoidal MMP
journal, February 2017
- Leão, Pedro; Chen, Yi-Ran; Abreu, Fernanda
- Environmental Microbiology, Vol. 19, Issue 6
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
Bacterial Biovolume and Biomass Estimations
journal, January 1985
- Bratbak, Gunnar
- Applied and Environmental Microbiology, Vol. 49, Issue 6
Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules.
text, January 2019
- Roth, Ronelle; Hillmer, Stefan; Funaya, Charlotta
- Apollo - University of Cambridge Repository
Concretionary methane-seep carbonates and associated microbial communities in Black Sea sediments
text, January 2005
- Reitner, J.; Peckmann, J.; Blumenberg, M.
- FID GEO
Deposition of biogenic iron minerals in a methane oxidizing microbial mat.
text, January 2013
- Wrede, Christoph; Kokoschka, Sebastian; Dreier, Anne
- FID GEO
Constraints on mechanisms and rates of anaerobic oxidation of methane by microbial consortia: process-based modeling of ANME-2 archaea and sulfate reducing bacteria interactions
journal, January 2008
- Orcutt, B.; Meile, C.
- Biogeosciences Discussions, Vol. 5, Issue 3
Works referencing / citing this record:
3D Analysis of Ordered Porous Polymeric Particles using Complementary Electron Microscopy Methods
journal, September 2019
- Alvarez, Juan; Saudino, Giovanni; Musteata, Valentina
- Scientific Reports, Vol. 9, Issue 1