Trace Metal Imaging of Sulfate-Reducing Bacteria and Methanogenic Archaea at Single-Cell Resolution by Synchrotron X-Ray Fluorescence Imaging

Glass, Jennifer B.; Chen, Si; Dawson, Katherine S.; Horton, Damian R.; Vogt, Stefan; Ingall, Ellery D.; Twining, Benjamin S.; Orphan, Victoria J.

doi:10.1080/01490451.2017.1321068

Title: Trace Metal Imaging of Sulfate-Reducing Bacteria and Methanogenic Archaea at Single-Cell Resolution by Synchrotron X-Ray Fluorescence Imaging

Journal Article · Fri Apr 21 00:00:00 EDT 2017 · Geomicrobiology Journal

DOI:https://doi.org/10.1080/01490451.2017.1321068· OSTI ID:1461422

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Georgia Inst. of Technology, Atlanta, GA (United States). School of Earth and Atmospheric Sciences
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source
California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)

Metal cofactors are required for many enzymes in anaerobic microbial respiration. This paper examined iron, cobalt, nickel, copper, and zinc in cellular and abiotic phases at the single-cell scale for a sulfate-reducing bacterium (Desulfococcus multivorans) and a methanogenic archaeon (Methanosarcina acetivorans) using synchrotron X-ray fluorescence microscopy. Relative abundances of cellular metals were also measured by inductively coupled plasma mass spectrometry. Finally, for both species, zinc and iron were consistently the most abundant cellular metals. M. acetivorans contained higher nickel and cobalt content than D. multivorans, likely due to elevated metal requirements for methylotrophic methanogenesis. Cocultures contained spheroid zinc sulfides and cobalt/copper sulfides.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States); California Institute of Technology (CalTech), Pasadena, CA (United States); Georgia Institute of Technology, Atlanta, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Aeronautics and Space Administration (NASA); National Science Foundation (NSF); Michigan Economic Development Corporation (United States); Michigan Technology Tri-Corridor (United States)

Grant/Contract Number:: AC02-06CH11357; SC0004949; NNX14AJ87G; OCE-0939564; 085P1000817

OSTI ID:: 1461422

Journal Information:: Geomicrobiology Journal, Vol. 35, Issue 1; ISSN 0149-0451

Publisher:: Taylor & FrancisCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 9 works

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References (80)

Effect of cobalt on the anaerobic thermophilic conversion of methanol Paulo, Paula L.; Jiang, Bo; Cysneiros, Denise Biotechnology and Bioengineering, Vol. 85, Issue 4 https://doi.org/10.1002/bit.10876	journal	January 2004
Nickel-Containing Carbon Monoxide Dehydrogenase/Acetyl-CoA Synthase^, Ragsdale, Stephen W.; Kumar, Manoj Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950058+	journal	January 1996
Interactions of exopolymers produced by sulphate-reducing bacteria with metal ions Beech, I. B.; Cheung, C. W. S. International Biodeterioration & Biodegradation, Vol. 35, Issue 1-3 https://doi.org/10.1016/0964-8305(95)00082-G	journal	January 1995
The bacterial metallome: composition and stability with specific reference to the anaerobic bacterium Desulfovibrio desulfuricans Barton, Larry L.; Goulhen, Florence; Bruschi, Mireille BioMetals, Vol. 20, Issue 3-4 https://doi.org/10.1007/s10534-006-9059-2	journal	January 2007
Differences in Hydrogenase Gene Expression between Methanosarcina acetivorans and Methanosarcina barkeri Guss, A. M.; Kulkarni, G.; Metcalf, W. W. Journal of Bacteriology, Vol. 191, Issue 8 https://doi.org/10.1128/JB.00563-08	journal	February 2009
Dehalogenation of Chlorinated Ethenes and Immobilization of Nickel in Anaerobic Sediment Columns under Sulfidogenic Conditions Drzyzga, Oliver; El Mamouni, Rachid; Agathos, Spiros N. Environmental Science & Technology, Vol. 36, Issue 12 https://doi.org/10.1021/es010184x	journal	June 2002
Elemental and Redox Analysis of Single Bacterial Cells by X-ray Microbeam Analysis Kemner, K. M. Science, Vol. 306, Issue 5696 https://doi.org/10.1126/science.1103524	journal	October 2004
Role of biogenic silica in the removal of iron from the Antarctic seas Ingall, Ellery D.; Diaz, Julia M.; Longo, Amelia F. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2981	journal	June 2013
Highly-defective nanocrystals of ZnS formed via dissimilatory bacterial sulfate reduction: A comparative study with their abiogenic analogues Xu, Jie; Murayama, Mitsuhiro; Roco, Charles M. Geochimica et Cosmochimica Acta, Vol. 180 https://doi.org/10.1016/j.gca.2016.02.007	journal	May 2016
Metal Sulfide Cluster Complexes and their Biogeochemical Importance in the Environment Luther, George W.; Rickard, David T. Journal of Nanoparticle Research, Vol. 7, Issue 4-5 https://doi.org/10.1007/s11051-005-4272-4	journal	October 2005
Methanogens, sulphate and heavy metals: a complex system Paulo, Lara M.; Stams, Alfons J. M.; Sousa, Diana Z. Reviews in Environmental Science and Bio/Technology, Vol. 14, Issue 4 https://doi.org/10.1007/s11157-015-9387-1	journal	November 2015
Trace Metal Requirements for Microbial Enzymes Involved in the Production and Consumption of Methane and Nitrous Oxide Glass, Jennifer B.; Orphan, Victoria J. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00061	journal	January 2012
Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments: Metal micronutrients for anaerobic oxidation of methane Glass, Jennifer B.; Yu, Hang; Steele, Joshua A. Environmental Microbiology, Vol. 16, Issue 6 https://doi.org/10.1111/1462-2920.12314	journal	November 2013
Composition of the major elements and trace elements of 10 methanogenic bacteria determined by inductively coupled plasma emission spectrometry Scherer, P.; Lippert, H.; Wolff, G. Biological Trace Element Research, Vol. 5, Issue 3 https://doi.org/10.1007/BF02916619	journal	June 1983
Hemoproteins in Dissimilatory Sulfate- and Sulfur-Reducing Prokaryotes Fauque, Guy D.; Barton, Larry L. Advances in Microbial Physiology https://doi.org/10.1016/B978-0-12-398264-3.00001-2	book	January 2012
Immobilization of Cobalt by Sulfate-Reducing Bacteria in Subsurface Sediments Krumholz, Lee R.; Elias, Dwayne A.; Suflita, Joseph M. Geomicrobiology Journal, Vol. 20, Issue 1 https://doi.org/10.1080/01490450303892	journal	January 2003
Exploring Ocean Biogeochemistry by Single-Cell Microprobe Analysis of Protist Elemental Composition Twining, Benjamin S.; Baines, Stephen B.; Vogt, Stefan Journal of Eukaryotic Microbiology, Vol. 55, Issue 3 https://doi.org/10.1111/j.1550-7408.2008.00320.x	journal	May 2008
Electron transfer in syntrophic communities of anaerobic bacteria and archaea Stams, Alfons J. M.; Plugge, Caroline M. Nature Reviews Microbiology, Vol. 7, Issue 8 https://doi.org/10.1038/nrmicro2166	journal	August 2009
Quantifying Trace Elements in Individual Aquatic Protist Cells with a Synchrotron X-ray Fluorescence Microprobe Twining, Benjamin S.; Baines, Stephen B.; Fisher, Nicholas S. Analytical Chemistry, Vol. 75, Issue 15 https://doi.org/10.1021/ac034227z	journal	August 2003
Methanol conversion in high-rate anaerobic reactors Weijma, J.; Stams, A. J. M. Water Science and Technology, Vol. 44, Issue 8 https://doi.org/10.2166/wst.2001.0452	journal	October 2001
Ultrastructure, aggregation-state, and crystal growth of biogenic nanocrystalline sphalerite and wurtzite Moreau, John W.; Webb, Richard I.; Banfield, Jillian F. American Mineralogist, Vol. 89, Issue 7 https://doi.org/10.2138/am-2004-0704	journal	July 2004
Insight into the mechanism of biological methanol activation based on the crystal structure of the methanol-cobalamin methyltransferase complex Hagemeier, C. H.; Krer, M.; Thauer, R. K. Proceedings of the National Academy of Sciences, Vol. 103, Issue 50 https://doi.org/10.1073/pnas.0603650103	journal	December 2006
Single cell activity reveals direct electron transfer in methanotrophic consortia McGlynn, Shawn E.; Chadwick, Grayson L.; Kempes, Christopher P. Nature, Vol. 526, Issue 7574 https://doi.org/10.1038/nature15512	journal	September 2015
A new type of metal-binding site in cobalt- and zinc-containing adenylate kinases isolated from sulfate-reducers Desulfovibrio gigas and Desulfovibrio desulfuricans ATCC 27774 Gavel, Olga Yu.; Bursakov, Sergey A.; Rocco, Giulia Di Journal of Inorganic Biochemistry, Vol. 102, Issue 5-6 https://doi.org/10.1016/j.jinorgbio.2008.01.023	journal	May 2008
Formation of Ni- and Zn-Sulfides in Cultures of Sulfate-Reducing Bacteria Gramp, Jonathan P.; Bigham, Jerry M.; Sasaki, Keiko Geomicrobiology Journal, Vol. 24, Issue 7-8 https://doi.org/10.1080/01490450701758239	journal	December 2007
A Cysteine-Rich CCG Domain Contains a Novel [4Fe-4S] Cluster Binding Motif As Deduced from Studies with Subunit B of Heterodisulfide Reductase from Methanothermobacter marburgensis ^† Hamann, Nils; Mander, Gerd J.; Shokes, Jacob E. Biochemistry, Vol. 46, Issue 44 https://doi.org/10.1021/bi700679u	journal	November 2007
Extracellular Proteins Limit the Dispersal of Biogenic Nanoparticles Moreau, J. W.; Weber, P. K.; Martin, M. C. Science, Vol. 316, Issue 5831 https://doi.org/10.1126/science.1141064	journal	June 2007
Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence? Ozuolmez, Derya; Na, Hyunsoo; Lever, Mark A. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00492	journal	May 2015
How to Make a Living by Exhaling Methane Ferry, James G. Annual Review of Microbiology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev.micro.112408.134051	journal	October 2010
The Bionanoprobe: hard X-ray fluorescence nanoprobe with cryogenic capabilities Chen, S.; Deng, J.; Yuan, Y. Journal of Synchrotron Radiation, Vol. 21, Issue 1 https://doi.org/10.1107/S1600577513029676	journal	December 2013
Trace element requirements of agricultural biogas digesters during biological conversion of renewable biomass to methane Demirel, B.; Scherer, P. Biomass and Bioenergy, Vol. 35, Issue 3 https://doi.org/10.1016/j.biombioe.2010.12.022	journal	March 2011
Cobalt Limitation of Growth and Mercury Methylation in Sulfate-Reducing Bacteria Ekstrom, Eileen B.; Morel, François M. M. Environmental Science & Technology, Vol. 42, Issue 1, p. 93-99 https://doi.org/10.1021/es0705644	journal	January 2008
Structure of an F430 Variant from Archaea Associated with Anaerobic Oxidation of Methane Mayr, Stefan; Latkoczy, Christopher; Krüger, Martin Journal of the American Chemical Society, Vol. 130, Issue 32 https://doi.org/10.1021/ja802929z	journal	August 2008
Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals Fahrni, Christoph J. Current Opinion in Chemical Biology, Vol. 11, Issue 2 https://doi.org/10.1016/j.cbpa.2007.02.039	journal	April 2007
Quantifying Heavy Metals Sequestration by Sulfate-Reducing Bacteria in an Acid Mine Drainage-Contaminated Natural Wetland Moreau, John W.; Fournelle, John H.; Banfield, Jillian F. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00043	journal	January 2013
Cobalt sorption onto anaerobic granular sludge: Isotherm and spatial localization analysis van Hullebusch, Eric D.; Gieteling, Jarno; Zhang, Min Journal of Biotechnology, Vol. 121, Issue 2 https://doi.org/10.1016/j.jbiotec.2005.07.011	journal	January 2006
Granular sludge in full-scale anaerobic bioreactors: Trace element content and deficiencies Zandvoort, Marcel H.; van Hullebusch, Eric D.; Gieteling, Jarno Enzyme and Microbial Technology, Vol. 39, Issue 2 https://doi.org/10.1016/j.enzmictec.2006.03.034	journal	June 2006
Formation of Covellite (CuS) Under Biological Sulfate-Reducing Conditions Gramp, Jonathan P.; Sasaki, Keiko; Bigham, Jerry M. Geomicrobiology Journal, Vol. 23, Issue 8 https://doi.org/10.1080/01490450600964383	journal	December 2006
Speciation of Co(II) and Ni(II) in Anaerobic Bioreactors Measured by Competitive Ligand Exchange−Adsorptive Stripping Voltammetry Jansen, Stefan; Steffen, Fraukje; Threels, Wim F. Environmental Science & Technology, Vol. 39, Issue 24 https://doi.org/10.1021/es050492l	journal	December 2005
Nanocrystalline Nickel and Cobalt Sulfides Formed by a Heavy Metal-Tolerant, Sulfate-Reducing Enrichment Culture Sitte, Jana; Pollok, Kilian; Langenhorst, Falko Geomicrobiology Journal, Vol. 30, Issue 1 https://doi.org/10.1080/01490451.2011.653082	journal	January 2013
Crystal Structure of Methyl-Coenzyme M Reductase: The Key Enzyme of Biological Methane Formation Ermler, U. Science, Vol. 278, Issue 5342 https://doi.org/10.1126/science.278.5342.1457	journal	November 1997
Biofilm growth mode promotes maximum carrying capacity and community stability during product inhibition syntrophy Brileya, Kristen A.; Camilleri, Laura B.; Zane, Grant M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00693	journal	December 2014
Methanol degradation in granular sludge reactors at sub-optimal metal concentrations: role of iron, nickel and cobalt Zandvoort, Marcel H.; Geerts, Roy; Lettinga, Gatze Enzyme and Microbial Technology, Vol. 33, Issue 2-3 https://doi.org/10.1016/S0141-0229(03)00114-5	journal	August 2003
Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis Outten, C. E. Science, Vol. 292, Issue 5526 https://doi.org/10.1126/science.1060331	journal	June 2001
Quantitative Fluorescence In Situ Hybridization Analysis of Microbial Consortia from a Biogenic Gas Field in Alaska's Cook Inlet Basin Dawson, Katherine S.; Strąpoć, Dariusz; Huizinga, Brad Applied and Environmental Microbiology, Vol. 78, Issue 10 https://doi.org/10.1128/AEM.07122-11	journal	March 2012
Hydrogen ?leakage? during methanogenesis from methanol and methylamine: implications for anaerobic carbon degradation pathways in aquatic sediments Finke, Niko; Hoehler, Tori Michael; Jørgensen, Bo Barker Environmental Microbiology, Vol. 9, Issue 4 https://doi.org/10.1111/j.1462-2920.2007.01248.x	journal	April 2007
Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment Loy, A.; Lehner, A.; Lee, N. Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.5064-5081.2002	journal	October 2002
Fractionation of Hydrogen Isotopes by Sulfate- and Nitrate-Reducing Bacteria Osburn, Magdalena R.; Dawson, Katherine S.; Fogel, Marilyn L. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01166	journal	August 2016
The impact of Co and Ni speciation on methanogenesis in sulfidic media—Biouptake versus metal dissolution Jansen, Stefan; Gonzalez-Gil, Graciela; van Leeuwen, Herman P. Enzyme and Microbial Technology, Vol. 40, Issue 4 https://doi.org/10.1016/j.enzmictec.2006.06.019	journal	March 2007
Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Dominant Microbial Populations in Limestone-Corroding Stream Biofilms, Frasassi Cave System, Italy Macalady, J. L.; Lyon, E. H.; Koffman, B. Applied and Environmental Microbiology, Vol. 72, Issue 8 https://doi.org/10.1128/AEM.00715-06	journal	August 2006
Essential metals for nitrogen fixation in a free-living N ₂ -fixing bacterium: chelation, homeostasis and high use efficiency : Homeostasis of nitrogenase metal cofactors in Bellenger, J. -P.; Wichard, T.; Xu, Y. Environmental Microbiology, Vol. 13, Issue 6 https://doi.org/10.1111/j.1462-2920.2011.02440.x	journal	March 2011
Gold-FISH: A new approach for the in situ detection of single microbial cells combining fluorescence and scanning electron microscopy Schmidt, Hannes; Eickhorst, Thilo; Mußmann, Marc Systematic and Applied Microbiology, Vol. 35, Issue 8 https://doi.org/10.1016/j.syapm.2012.04.006	journal	December 2012
Study of the interaction of sulphate-reducing bacteria exopolymers with iron using X-ray photoelectron spectroscopy and time-of-flight secondary ionisation mass spectrometry Beech, I. B.; Zinkevich, V.; Tapper, R. Journal of Microbiological Methods, Vol. 36, Issue 1-2 https://doi.org/10.1016/S0167-7012(99)00005-6	journal	May 1999
ATP Sulfurylases from Sulfate-Reducing Bacteria of the Genus Desulfovibrio. A Novel Metalloprotein Containing Cobalt and Zinc ^† Gavel, Olga Yu.; Bursakov, Sergey A.; Calvete, Juan J. Biochemistry, Vol. 37, Issue 46 https://doi.org/10.1021/bi9816709	journal	November 1998
dbTEU: a protein database of trace element utilization Zhang, Yan; Gladyshev, Vadim N. Bioinformatics, Vol. 26, Issue 5 https://doi.org/10.1093/bioinformatics/btp705	journal	January 2010
Extracellular metal-binding activity of the sulphate-reducing bacterium Desulfococcus multivorans Gadd, Geoffrey M.; White, Chris; Bridge, Toni A. M. Microbiology, Vol. 145, Issue 10 https://doi.org/10.1099/00221287-145-10-2987	journal	October 1999
Modelling the competition between sulphate reducers and methanogens in a thermophilic methanol-fed bioreactor Spanjers, H.; Weijma, J.; Abusam, A. Water Science and Technology, Vol. 45, Issue 10 https://doi.org/10.2166/wst.2002.0299	journal	May 2002
Hydrogenases from Methanogenic Archaea, Nickel, a Novel Cofactor, and H ₂ Storage Thauer, Rudolf K.; Kaster, Anne-Kristin; Goenrich, Meike Annual Review of Biochemistry, Vol. 79, Issue 1 https://doi.org/10.1146/annurev.biochem.030508.152103	journal	June 2010
The Unique Biogeochemical Signature of the Marine Diazotroph Trichodesmium Nuester, Jochen; Vogt, Stefan; Newville, Matthew Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00150	journal	January 2012
Effect of trace elements and vitamins on the growth of Methanosarcina barkeri Scherer, P.; Sahm, H. Acta Biotechnologica, Vol. 1, Issue 1 https://doi.org/10.1002/abio.370010108	journal	January 1981
Ecological Aspects of the Distribution of Different Autotrophic CO ₂ Fixation Pathways Berg, Ivan A. Applied and Environmental Microbiology, Vol. 77, Issue 6 https://doi.org/10.1128/AEM.02473-10	journal	January 2011
Nickel and cobalt sorption on anaerobic granular sludges: kinetic and equilibrium studies van Hullebusch, Eric D.; Zandvoort, Marcel H.; Lens, Piet NL Journal of Chemical Technology & Biotechnology, Vol. 79, Issue 11 https://doi.org/10.1002/jctb.1116	journal	October 2004
Metabolic associations with archaea drive shifts in hydrogen isotope fractionation in sulfate-reducing bacterial lipids in cocultures and methane seeps Dawson, K. S.; Osburn, M. R.; Sessions, A. L. Geobiology, Vol. 13, Issue 5 https://doi.org/10.1111/gbi.12140	journal	April 2015
Microbial metalloproteomes are largely uncharacterized Cvetkovic, Aleksandar; Menon, Angeli Lal; Thorgersen, Michael P. Nature, Vol. 466, Issue 7307 https://doi.org/10.1038/nature09265	journal	July 2010
Precipitation of Cu-Sulfides by Copper-Tolerant Desulfovibrio Isolates Karnachuk, Olia V.; Sasaki, Keiko; Gerasimchuk, Anna L. Geomicrobiology Journal, Vol. 25, Issue 5 https://doi.org/10.1080/01490450802153124	journal	June 2008
Sorption of cobalt and nickel on anaerobic granular sludges: isotherms and sequential extraction van Hullebusch, Eric D.; Peerbolte, Annemarie; Zandvoort, Marcel H. Chemosphere, Vol. 58, Issue 4 https://doi.org/10.1016/j.chemosphere.2004.09.017	journal	January 2005
Exopolymeric substances of sulfate-reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals Braissant, O.; Decho, A. W.; Dupraz, C. Geobiology, Vol. 5, Issue 4 https://doi.org/10.1111/j.1472-4669.2007.00117.x	journal	December 2007
A First Analysis of Metallome Biosignatures of Hyperthermophilic Archaea Cameron, Vyllinniskii; House, Christopher H.; Brantley, Susan L. Archaea, Vol. 2012 https://doi.org/10.1155/2012/789278	journal	January 2012
Effects of Nickel and Cobalt on Kinetics of Methanol Conversion by Methanogenic Sludge as Assessed by On-Line CH4 Monitoring Gonzalez-Gil, Graciela; Kleerebezem, Robbert; Lettinga, Gatze Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1789-1793.1999	journal	April 1999
Methanogenesis and Sulfate Reduction: Competitive and Noncompetitive Substrates in Estuarine Sediments Oremland, Ronald S.; Polcin, Sandra Applied and Environmental Microbiology, Vol. 44, Issue 6 https://doi.org/10.1128/AEM.44.6.1270-1276.1982	journal	January 1982
Quantification of methanogenic groups in anaerobic biological reactors by oligonucleotide probe hybridization. Raskin, L.; Poulsen, L. K.; Noguera, D. R. Applied and Environmental Microbiology, Vol. 60, Issue 4 https://doi.org/10.1128/AEM.60.4.1241-1248.1994	journal	January 1994
Interactions of exopolymers produced by sulphate-reducing bacteria with metal ions Beech, I. B.; Cheung, W. S. International Biodeterioration & Biodegradation, Vol. 35, Issue 1-3 https://doi.org/10.1016/0964-8305(95)90028-4	journal	January 1995
Methanogenic archaea and sulfate reducing bacteria co-cultured on acetate: teamwork or coexistence? Ozuolmez, Derya; Na, Hyunsoo; Lever, Mark A. ETH Zurich https://doi.org/10.3929/ethz-b-000103148	text	January 2015
Handbook of microbiological media [Review] Choice Reviews Online, Vol. 31, Issue 10, 31-5434 https://doi.org/10.5860/choice.31-5434	journal	June 1994
Effect of cobalt on the anaerobic degradation of methanol Florencio, Lourdinha; Jeniček, Pavel; Field, Jim A. Journal of Fermentation and Bioengineering, Vol. 75, Issue 5 https://doi.org/10.1016/0922-338x(93)90136-v	journal	January 1993
Sulfate-Dependent Interspecies H2 Transfer between Methanosarcina barkeri and Desulfovibrio vulgaris during Coculture Metabolism of Acetate or Methanol Phelps, T. J.; Conrad, R.; Zeikus, J. G. Applied and Environmental Microbiology, Vol. 50, Issue 3 https://doi.org/10.1128/aem.50.3.589-594.1985	journal	January 1985
Importance of cobalt for individual trophic groups in an anaerobic methanol-degrading consortium. Florencio, L.; Field, J. A.; Lettinga, G. Applied and Environmental Microbiology, Vol. 60, Issue 1 https://doi.org/10.1128/aem.60.1.227-234.1994	journal	January 1994
Spectrochemical Analysis of Inorganic Elements in Bacteria Rouf, M. A. Journal of Bacteriology, Vol. 88, Issue 6 https://doi.org/10.1128/jb.88.6.1545-1549.1964	journal	January 1964
Effect of trace elements and vitamins on the growth of Methanosarcina barkeri Scherer, P.; Sahm, H. Acta Biotechnologica https://doi.org/10.1515/9783112543429-008	book	December 1981

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59 BASIC BIOLOGICAL SCIENCES
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