Diversity and distribution of methanotrophic archaea at cold seeps.
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Journal: 2005/March - Applied and Environmental Microbiology
ISSN: 0099-2240
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In this study we investigated by using 16S rRNA-based methods the distribution and biomass of archaea in samples from (i) sediments above outcropping methane hydrate at Hydrate Ridge (Cascadia margin off Oregon) and (ii) massive microbial mats enclosing carbonate reefs (Crimea area, Black Sea). The archaeal diversity was low in both locations; there were only four (Hydrate Ridge) and five (Black Sea) different phylogenetic clusters of sequences, most of which belonged to the methanotrophic archaea (ANME). ANME group 2 (ANME-2) sequences were the most abundant and diverse sequences at Hydrate Ridge, whereas ANME-1 sequences dominated the Black Sea mats. Other seep-specific sequences belonged to the newly defined group ANME-3 (related to Methanococcoides spp.) and to the Crenarchaeota of marine benthic group B. Quantitative analysis of the samples by fluorescence in situ hybridization (FISH) showed that ANME-1 and ANME-2 co-occurred at the cold seep sites investigated. At Hydrate Ridge the surface sediments were dominated by aggregates consisting of ANME-2 and members of the Desulfosarcina-Desulfococcus branch (DSS) (ANME-2/DSS aggregates), which accounted for >90% of the total cell biomass. The numbers of ANME-1 cells increased strongly with depth; these cells accounted 1% of all single cells at the surface and more than 30% of all single cells (5% of the total cells) in 7- to 10-cm sediment horizons that were directly above layers of gas hydrate. In the Black Sea microbial mats ANME-1 accounted for about 50% of all cells. ANME-2/DSS aggregates occurred in microenvironments within the mat but accounted for only 1% of the total cells. FISH probes for the ANME-2a and ANME-2c subclusters were designed based on a comparative 16S rRNA analysis. In Hydrate Ridge sediments ANME-2a/DSS and ANME-2c/DSS aggregates differed significantly in morphology and abundance. The relative abundance values for these subgroups were remarkably different at Beggiatoa sites (80% ANME-2a, 20% ANME-2c) and Calyptogena sites (20% ANME-2a, 80% ANME-2c), indicating that there was preferential selection of the groups in the two habitats. These variations in the distribution, diversity, and morphology of methanotrophic consortia are discussed with respect to the presence of microbial ecotypes, niche formation, and biogeography.
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Appl Environ Microbiol 71(1): 467-479
PMID: 15640223

Diversity and Distribution of Methanotrophic Archaea at Cold Seeps<sup><a href="#fn1" rid="fn1" class=" fn">†</a></sup>

Max Planck Institute for Marine Microbiology, International University of Bremen, Bremen, ICBM-Geomicrobiology Group, University of Oldenburg, Oldenburg, Germany3
Corresponding author. Mailing address: Max Planck Institute for Marine Microbiology, Department of Molecular Ecology, Celsiusstrasse 1, 28359 Bremen, Germany. Phone: 49-421-2028936. Fax: 49-421-2028580. E-mail: ed.nemerb-ipm@lettinkk.
Received 2004 Apr 16; Accepted 2004 Aug 10.
Copyright © 2005, American Society for Microbiology

Abstract

In this study we investigated by using 16S rRNA-based methods the distribution and biomass of archaea in samples from (i) sediments above outcropping methane hydrate at Hydrate Ridge (Cascadia margin off Oregon) and (ii) massive microbial mats enclosing carbonate reefs (Crimea area, Black Sea). The archaeal diversity was low in both locations; there were only four (Hydrate Ridge) and five (Black Sea) different phylogenetic clusters of sequences, most of which belonged to the methanotrophic archaea (ANME). ANME group 2 (ANME-2) sequences were the most abundant and diverse sequences at Hydrate Ridge, whereas ANME-1 sequences dominated the Black Sea mats. Other seep-specific sequences belonged to the newly defined group ANME-3 (related to Methanococcoides spp.) and to the Crenarchaeota of marine benthic group B. Quantitative analysis of the samples by fluorescence in situ hybridization (FISH) showed that ANME-1 and ANME-2 co-occurred at the cold seep sites investigated. At Hydrate Ridge the surface sediments were dominated by aggregates consisting of ANME-2 and members of the Desulfosarcina-Desulfococcus branch (DSS) (ANME-2/DSS aggregates), which accounted for >90% of the total cell biomass. The numbers of ANME-1 cells increased strongly with depth; these cells accounted 1% of all single cells at the surface and more than 30% of all single cells (5% of the total cells) in 7- to 10-cm sediment horizons that were directly above layers of gas hydrate. In the Black Sea microbial mats ANME-1 accounted for about 50% of all cells. ANME-2/DSS aggregates occurred in microenvironments within the mat but accounted for only 1% of the total cells. FISH probes for the ANME-2a and ANME-2c subclusters were designed based on a comparative 16S rRNA analysis. In Hydrate Ridge sediments ANME-2a/DSS and ANME-2c/DSS aggregates differed significantly in morphology and abundance. The relative abundance values for these subgroups were remarkably different at Beggiatoa sites (80% ANME-2a, 20% ANME-2c) and Calyptogena sites (20% ANME-2a, 80% ANME-2c), indicating that there was preferential selection of the groups in the two habitats. These variations in the distribution, diversity, and morphology of methanotrophic consortia are discussed with respect to the presence of microbial ecotypes, niche formation, and biogeography.

Abstract

The microbially mediated anaerobic oxidation of methane (AOM) is the major biological sink of the greenhouse gas methane in marine sediments (49) and serves as an important control for emission of methane into the hydrosphere. The AOM metabolic process is assumed to be a reversal of methanogenesis coupled to the reduction of sulfate to sulfide involving methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) as syntrophic partners (7, 20, 21, 23, 69). Neither the ANME groups nor their sulfate-reducing partners have been isolated yet, and the enzymes and biochemical pathways involved in AOM remain unknown (18, 19). Very recently, however, Krüger et al. described a candidate enzyme (Ni-protein I) that may catalyze methane activation in a reverse terminal methyl-coenzyme M reductase reaction (27), supporting the hypothesis that reverse methanogenesis occurs in the ANME groups. Field and laboratory studies have provided ample evidence that AOM can be mediated by structured consortia consisting of archaea (ANME group 2 [ANME-2]) belonging to the order Methanosarcinales and SRB belonging to the Desulfosarcina-Desulfococcus branch (DSS) of the Deltaproteobacteria (7, 40); below these consortia are referred to as ANME-2/DSS aggregates. These consortia oxidize methane with sulfate, yielding equimolar amounts of carbonate and sulfide (37). A second archaeal group (ANME-1), which is distantly related to the Methanosarcinales and Methanomicrobiales, has also been shown to mediate AOM (34, 41). Using fluorescence in situ hybridization (FISH) combined with secondary ion mass spectrometry, Orphan and coworkers were able to measure carbon isotopic signatures of single aggregates of ANME-1 and ANME-2 cells (40, 41). Their δC values were extremely low and thus provided direct evidence for methanotrophy in both phylogenetic clusters. At hot spot sites of AOM in different marine environments phylogenetic analyses based on 16S rRNA gene sequencing of microbial communities showed that there was relatively low diversity of archaea compared to the bacterial diversity in these habitats (21, 26, 28, 39, 58) (GenBank accession numbers {"type":"entrez-nucleotide","attrs":{"text":"AY593257","term_id":"50402591","term_text":"AY593257"}}AY593257 to {"type":"entrez-nucleotide","attrs":{"text":"AY593349","term_id":"50402683","term_text":"AY593349"}}AY593349 and {"type":"entrez-nucleotide","attrs":{"text":"AF357889","term_id":"23957188","term_text":"AF357889"}}AF357889 to {"type":"entrez-nucleotide","attrs":{"text":"AF361694","term_id":"19850621","term_text":"AF361694"}}AF361694 [http://www.ncbi.nlm.nih.gov]) and indicated the co-occurrence of several ANME-1 and ANME-2 populations. However, such studies so far have not provided quantification of the biomasses of the different groups and their distribution in the environment.

The presence of several microbial populations with essentially the same function in a given environment is still a major puzzle in our concept of biodiversity and microbial ecology. In this study we dealt with methanotrophic archaea, which are limited to extreme environments with anoxic, methane-rich, and sulfate-containing sediments. Hence, the rest of the ocean represents a barrier to the dispersal of these organisms, making them an interesting case study for the central question of microbial biogeography, which is “Is everything everywhere?” (3, 5, 15, 71). To find clues to potential niche occupation by the different ANME groups, we investigated the phylogenetic diversity, distribution, and abundance of the methanotrophs at selected seep sites with high rates of AOM (34, 65), including sediments from three different types of chemosynthetic communities (Beggiatoa mats, Calyptogena fields, and Acharax fields) above outcropping methane hydrate at Hydrate Ridge (Cascadia margin off Oregon) and massive methanotrophic microbial mats at Black Sea methane seeps.

Acknowledgments

We thank the officers, crews, and shipboard scientific parties of R/V SONNE during TECFLUX cruises SO143 and SO148 (grants 03G0143A and 03G0148A) to Hydrate Ridge and during the GHOSTDABS cruise (grant 03G0559A) of R/V Prof. LOGACHEV in summer 2001 for their excellent support. We acknowledge GEOTECHNOLOGIEN projects OMEGA (grant 03G0566A), LOTUS (grant 03G0565), and GHOSTDABS for providing access to samples and infrastructure. We are indebted to Doug Bartlett, Sander Heijs, Brian Lanoil, and Andreas Teske for sharing their sequence data prior to publication for probe construction. Armin Gieseke is acknowledged for providing an introduction to laser scanning microscopy, and Julia Polansky and Andreas Lemke are acknowledged for technical assistance.

This study was part of the program MUMM (Mikrobielle Umsatzraten von Methan in gashydrathaltigen Sedimenten; grant 03G0554A) supported by the Bundesministerium für Bildung und Forschung (Germany). Further support was provided by the Max Planck Society, Germany.

Acknowledgments

Footnotes

Publication GEOTECH-85 of the GEOTECHNOLOGIEN program and no. 10 of the research program GHOSTDABS of the Bundesministerium für Bildung und Forschung and the DFG.

Footnotes

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