Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Methane-Consuming Archaea Revealed by Directly Coupled Isotopic and Phylogenetic Analysis
Victoria J. Orphan,1*Christopher H. House,2*Kai-Uwe Hinrichs,3Kevin D. McKeegan,4Edward F. DeLong1
Microorganisms living in anoxic marine sediments consume
more than 80% of the methane produced in the world's oceans. In
additionto single-species aggregates, consortia of metabolically
interdependentbacteria and archaea are found in methane-rich
sediments. A combinationof fluorescence in situ hybridization and
secondary ion mass spectrometryshows that cells belonging to one
specific archaeal group associatedwith the
Methanosarcinales were all highly depleted in
13C (to values of -96). This depletion indicates
assimilation ofisotopically light methane into specific archaeal
cells. Additionalmicrobial species apparently use other carbon
sources, as indicatedby significantly higher
13C/12C ratios in their cell carbon. Our
results demonstrate the feasibilityof simultaneous determination of
the identity and the metabolicactivity of naturally occurring
microorganisms.
1 Monterey Bay Aquarium Research Institute,
Moss Landing, CA 95039, USA.
2 Department of
Geosciences, The Pennsylvania State University, University Park, PA
16802, USA.
3 Department of Geology and Geophysics,
Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
4 Department of Earth and Space Sciences, University
of California, Los Angeles, CA 90095, USA.
*
These authors contributed equally to the work.
To whom correspondence should be addressed. E-mail:
chouse{at}geosc.psu.edu and delong{at}mbari.org
The editors suggest the following Related Resources on Science sites:
In Science Magazine
NEWS FOCUS
Carl Zimmer (20 July 2001) Science293 (5529), 418.
[DOI: 10.1126/science.293.5529.418] |Summary »|Full Text »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Linking Microbial Phylogeny to Metabolic Activity at the Single-Cell Level by Using Enhanced Element Labeling-Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (EL-FISH) and NanoSIMS.
S. Behrens, T. Losekann, J. Pett-Ridge, P. K. Weber, W.-O. Ng, B. S. Stevenson, I. D. Hutcheon, D. A. Relman, and A. M. Spormann (2008)
Appl. Envir. Microbiol.
74, 3143-3150
|Abstract »|Full Text »|PDF »
Physiology, Ecology, Phylogeny, and Genomics of Microorganisms Capable of Syntrophic Metabolism.
M. J. MCINERNEY, C. G. STRUCHTEMEYER, J. SIEBER, H. MOUTTAKI, A. J. M. STAMS, B. SCHINK, L. ROHLIN, and R. P. GUNSALUS (2008)
Ann. N.Y. Acad. Sci.
1125, 58-72
|Abstract »|Full Text »|PDF »
Quantifying Microbial Utilization of Petroleum Hydrocarbons in Salt Marsh Sediments by Using the 13C Content of Bacterial rRNA.
A. Pearson, K. S. Kraunz, A. L. Sessions, A. E. Dekas, W. D. Leavitt, and K. J. Edwards (2008)
Appl. Envir. Microbiol.
74, 1157-1166
|Abstract »|Full Text »|PDF »
Stable Isotope Ratios and Forensic Analysis of Microorganisms.
H. W. Kreuzer-Martin and K. H. Jarman (2007)
Appl. Envir. Microbiol.
73, 3896-3908
|Abstract »|Full Text »|PDF »
Diversity and Abundance of Aerobic and Anaerobic Methane Oxidizers at the Haakon Mosby Mud Volcano, Barents Sea.
T. Losekann, K. Knittel, T. Nadalig, B. Fuchs, H. Niemann, A. Boetius, and R. Amann (2007)
Appl. Envir. Microbiol.
73, 3348-3362
|Abstract »|Full Text »|PDF »
The genome of Syntrophus aciditrophicus: Life at the thermodynamic limit of microbial growth.
M. J. McInerney, L. Rohlin, H. Mouttaki, U. Kim, R. S. Krupp, L. Rios-Hernandez, J. Sieber, C. G. Struchtemeyer, A. Bhattacharyya, J. W. Campbell, et al. (2007)
PNAS
104, 7600-7605
|Abstract »|Full Text »|PDF »
Consumption of Methane and CO2 by Methanotrophic Microbial Mats from Gas Seeps of the Anoxic Black Sea.
T. Treude, V. Orphan, K. Knittel, A. Gieseke, C. H. House, and A. Boetius (2007)
Appl. Envir. Microbiol.
73, 2271-2283
|Abstract »|Full Text »|PDF »
Stable Isotope Probing: Linking Functional Activity to Specific Members of Microbial Communities.
Fluorescent In Situ Hybridization and Micro-autoradiography Applied to Ecophysiology in Soil.
S. W. Rogers, T. B. Moorman, and S. K. Ong (2007)
Soil Sci. Soc. Am. J.
71, 620-631
|Abstract »|Full Text »|PDF »
Diversity of Archaea in Marine Sediments from Skan Bay, Alaska, Including Cultivated Methanogens, and Description of Methanogenium boonei sp. nov..
M. M. Kendall, G. D. Wardlaw, C. F. Tang, A. S. Bonin, Y. Liu, and D. L. Valentine (2007)
Appl. Envir. Microbiol.
73, 407-414
|Abstract »|Full Text »|PDF »
An Anaerobic Methane-Oxidizing Community of ANME-1b Archaea in Hypersaline Gulf of Mexico Sediments.
K. G. Lloyd, L. Lapham, and A. Teske (2006)
Appl. Envir. Microbiol.
72, 7218-7230
|Abstract »|Full Text »|PDF »
Late Archean rise of aerobic microbial ecosystems.
Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru.
J. F. Biddle, J. S. Lipp, M. A. Lever, K. G. Lloyd, K. B. Sorensen, R. Anderson, H. F. Fredricks, M. Elvert, T. J. Kelly, D. P. Schrag, et al. (2006)
PNAS
103, 3846-3851
|Abstract »|Full Text »|PDF »
Use of Field-Based Stable Isotope Probing To Identify Adapted Populations and Track Carbon Flow through a Phenol-Degrading Soil Microbial Community.
C. M. DeRito, G. M. Pumphrey, and E. L. Madsen (2005)
Appl. Envir. Microbiol.
71, 7858-7865
|Abstract »|Full Text »|PDF »
Fate of Heterotrophic Microbes in Pelagic Habitats: Focus on Populations.
Methanogen Diversity Evidenced by Molecular Characterization of Methyl Coenzyme M Reductase A (mcrA) Genes in Hydrothermal Sediments of the Guaymas Basin.
A. Dhillon, M. Lever, K. G. Lloyd, D. B. Albert, M. L. Sogin, and A. Teske (2005)
Appl. Envir. Microbiol.
71, 4592-4601
|Abstract »|Full Text »|PDF »
Introduction and overview: What do we know for sure?.
Diversity and Distribution of Methanotrophic Archaea at Cold Seeps.
K. Knittel, T. Losekann, A. Boetius, R. Kort, and R. Amann (2005)
Appl. Envir. Microbiol.
71, 467-479
|Abstract »|Full Text »|PDF »
What Genetics Offers Geobiology.
D. K. Newman and J. A. Gralnick (2005)
Reviews in Mineralogy and Geochemistry
59, 9-26
|Full Text »|PDF »
Building the Biomarker Tree of Life.
J. J. Brocks and A. Pearson (2005)
Reviews in Mineralogy and Geochemistry
59, 233-258
|Full Text »|PDF »
Characterization of C1-Metabolizing Prokaryotic Communities in Methane Seep Habitats at the Kuroshima Knoll, Southern Ryukyu Arc, by Analyzing pmoA, mmoX, mxaF, mcrA, and 16S rRNA Genes.
F. Inagaki, U. Tsunogai, M. Suzuki, A. Kosaka, H. Machiyama, K. Takai, T. Nunoura, K. H. Nealson, and K. Horikoshi (2004)
Appl. Envir. Microbiol.
70, 7445-7455
|Abstract »|Full Text »|PDF »
Reverse Methanogenesis: Testing the Hypothesis with Environmental Genomics.
S. J. Hallam, N. Putnam, C. M. Preston, J. C. Detter, D. Rokhsar, P. M. Richardson, and E. F. DeLong (2004)
Science
305, 1457-1462
|Abstract »|Full Text »|PDF »
Stable Carbon Isotope Ratios of Lipid Biomarkers of Sulfate-Reducing Bacteria.
K. L. Londry, L. L. Jahnke, and D. J. Des Marais (2004)
Appl. Envir. Microbiol.
70, 745-751
|Abstract »|Full Text »|PDF »
Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment.
C. O. Jeon, W. Park, P. Padmanabhan, C. DeRito, J. R. Snape, and E. L. Madsen (2003)
PNAS
100, 13591-13596
|Abstract »|Full Text »|PDF »
Growth and Methane Oxidation Rates of Anaerobic Methanotrophic Archaea in a Continuous-Flow Bioreactor.
P. R. Girguis, V. J. Orphan, S. J. Hallam, and E. F. DeLong (2003)
Appl. Envir. Microbiol.
69, 5472-5482
|Abstract »|Full Text »|PDF »
Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea.
S. J. Hallam, P. R. Girguis, C. M. Preston, P. M. Richardson, and E. F. DeLong (2003)
Appl. Envir. Microbiol.
69, 5483-5491
|Abstract »|Full Text »|PDF »
Genomic Markers of Ancient Anaerobic Microbial Pathways: Sulfate Reduction, Methanogenesis, and Methane Oxidation.
Respiration of 13C-Labeled Substrates Added to Soil in the Field and Subsequent 16S rRNA Gene Analysis of 13C-Labeled Soil DNA.
P. Padmanabhan, S. Padmanabhan, C. DeRito, A. Gray, D. Gannon, J. R. Snape, C. S. Tsai, W. Park, C. Jeon, and E. L. Madsen (2003)
Appl. Envir. Microbiol.
69, 1614-1622
|Abstract »|Full Text »|PDF »
Biogeochemical Evidence that Thermophilic Archaea Mediate the Anaerobic Oxidation of Methane.
S. Schouten, S. G. Wakeham, E. C. Hopmans, and J. S. Sinninghe Damste (2003)
Appl. Envir. Microbiol.
69, 1680-1686
|Abstract »|Full Text »|PDF »
Archaea and Their Potential Role in Human Disease.
P. B. Eckburg, P. W. Lepp, and D. A. Relman (2003)
Infect. Immun.
71, 591-596
|Full Text »|PDF »
RNA Stable Isotope Probing, a Novel Means of Linking Microbial Community Function to Phylogeny.
M. Manefield, A. S. Whiteley, R. I. Griffiths, and M. J. Bailey (2002)
Appl. Envir. Microbiol.
68, 5367-5373
|Abstract »|Full Text »|PDF »
Microbial Reefs in the Black Sea Fueled by Anaerobic Oxidation of Methane.
W. Michaelis, R. Seifert, K. Nauhaus, T. Treude, V. Thiel, M. Blumenberg, K. Knittel, A. Gieseke, K. Peterknecht, T. Pape, et al. (2002)
Science
297, 1013-1015
|Abstract »|Full Text »|PDF »
Exploration of Inorganic C and N Assimilation by Soil Microbes with Time-of-Flight Secondary Ion Mass Spectrometry.
J. B. Cliff, D. J. Gaspar, P. J. Bottomley, and D. D. Myrold (2002)
Appl. Envir. Microbiol.
68, 4067-4073
|Abstract »|Full Text »|PDF »
Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing.
S. Radajewski, G. Webster, D. S. Reay, S. A. Morris, P. Ineson, D. B. Nedwell, J. I. Prosser, and J. C. Murrell (2002)
Microbiology
148, 2331-2342
|Abstract »|Full Text »|PDF »
From the Cover: Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments.
V. J. Orphan, C. H. House, K.-U. Hinrichs, K. D. McKeegan, and E. F. DeLong (2002)
PNAS
99, 7663-7668
|Abstract »|Full Text »|PDF »
Geomicrobiology: How Molecular-Scale Interactions Underpin Biogeochemical Systems.
Mass wasting, methane venting, and biological communities on the Mendocino transform fault.
(2002)
Geology
30, 407-410
Microbial Diversity of Hydrothermal Sediments in the Guaymas Basin: Evidence for Anaerobic Methanotrophic Communities.
A. Teske, K.-U. Hinrichs, V. Edgcomb, A. de Vera Gomez, D. Kysela, S. P. Sylva, M. L. Sogin, and H. W. Jannasch (2002)
Appl. Envir. Microbiol.
68, 1994-2007
|Abstract »|Full Text »|PDF »
Identification of Bacteria Responsible for Ammonia Oxidation in Freshwater Aquaria.
P. C. Burrell, C. M. Phalen, and T. A. Hovanec (2001)
Appl. Envir. Microbiol.
67, 5791-5800
|Abstract »|Full Text »|PDF »