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Applied and Environmental Microbiology, April 2002, p. 1994-2007, Vol. 68, No. 4
0099-2240/02/$04.00+0 DOI: 10.1128/AEM.68.4.1994-2007.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
Microbial Diversity of Hydrothermal Sediments in the Guaymas Basin: Evidence for Anaerobic Methanotrophic Communities
Andreas Teske,1* Kai-Uwe Hinrichs,2 Virginia Edgcomb,3 Alvin de Vera Gomez,1 David Kysela,3 Sean P. Sylva,2 Mitchell L. Sogin,3 and Holger W. Jannasch
Biology Department,1
Geology and Geophysics Department, Woods Hole Oceanographic Institution,2
Marine Biological Laboratory, The Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Woods Hole, Massachusetts3
Received 27 September 2001/
Accepted 25 January 2002
Microbial communities in hydrothermally active sediments of the Guaymas Basin (Gulf of California, Mexico) were studied by using 16S rRNA sequencing and carbon isotopic analysis of archaeal and bacterial lipids. The Guaymas sediments harbored uncultured euryarchaeota of two distinct phylogenetic lineages within the anaerobic methane oxidation 1 (ANME-1) group, ANME-1a and ANME-1b, and of the ANME-2c lineage within the Methanosarcinales, both previously assigned to the methanotrophic archaea. The archaeal lipids in the Guaymas Basin sediments included archaeol, diagnostic for nonthermophilic euryarchaeota, and sn-2-hydroxyarchaeol, with the latter compound being particularly abundant in cultured members of the Methanosarcinales. The concentrations of these compounds were among the highest observed so far in studies of methane seep environments. The
-13C values of these lipids (
-13C = -89 to -58
) indicate an origin from anaerobic methanotrophic archaea. This molecular-isotopic signature was found not only in samples that yielded predominantly ANME-2 clones but also in samples that yielded exclusively ANME-1 clones. ANME-1 archaea therefore remain strong candidates for mediation of the anaerobic oxidation of methane. Based on 16S rRNA data, the Guaymas sediments harbor phylogenetically diverse bacterial populations, which show considerable overlap with bacterial populations of geothermal habitats and natural or anthropogenic hydrocarbon-rich sites. Consistent with earlier observations, our combined evidence from bacterial phylogeny and molecular-isotopic data indicates an important role of some novel deeply branching bacteria in anaerobic methanotrophy. Anaerobic methane oxidation likely represents a significant and widely occurring process in the trophic ecology of methane-rich hydrothermal vents. This study stresses a high diversity among communities capable of anaerobic oxidation of methane.
* Corresponding author. Mailing address: Woods Hole Oceanographic Institution, Biology Dept./Redfield Laboratory, Woods Hole, MA 02543. Phone: (508) 289-2305. Fax: (508) 457-2134. E-mail:
ateske{at}whoi.edu.
This is WHOI contribution 10624.
Deceased.
Applied and Environmental Microbiology, April 2002, p. 1994-2007, Vol. 68, No. 4
0099-2240/02/$04.00+0 DOI: 10.1128/AEM.68.4.1994-2007.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
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-
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-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
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69: 2765-2772
[Abstract]
[Full Text]
-
Teske, A., Dhillon, A., Sogin, M. L.
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204: 186-191
[Abstract]
[Full Text]
-
Schouten, S., Wakeham, S. G., Hopmans, E. C., Sinninghe Damste, J. S.
(2003). Biogeochemical Evidence that Thermophilic Archaea Mediate the Anaerobic Oxidation of Methane. Appl. Environ. Microbiol.
69: 1680-1686
[Abstract]
[Full Text]
-
Edgcomb, V. P., Kysela, D. T., Teske, A., de Vera Gomez, A., Sogin, M. L.
(2002). Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc. Natl. Acad. Sci. USA
99: 7658-7662
[Abstract]
[Full Text]
-
Orphan, V. J., House, C. H., Hinrichs, K.-U., McKeegan, K. D., DeLong, E. F.
(2002). From the Cover: Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc. Natl. Acad. Sci. USA
99: 7663-7668
[Abstract]
[Full Text]
-
Reysenbach, A.-L., Shock, E.
(2002). Merging Genomes with Geochemistry in Hydrothermal Ecosystems. Science
296: 1077-1082
[Abstract]
[Full Text]