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An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments.

ABSTRACT: Sediments overlying a brine pool methane seep in the Gulf of Mexico (Green Canyon 205) were analyzed using molecular and geochemical approaches to identify geochemical controls on microbial community composition and stratification. 16S rRNA gene and rRNA clone libraries, as well as mcrA gene clone libraries, showed that the archaeal community consists predominantly of ANME-1b methane oxidizers; no archaea of other ANME subgroups were found with general and group-specific PCR primers. The ANME-1b community was found in the sulfate-methane interface, where undersaturated methane concentrations of ca. 100 to 250 microM coexist with sulfate concentrations around 10 mM. Clone libraries of dsrAB genes and bacterial 16S rRNA genes show diversified sulfate-reducing communities within and above the sulfate-methane interface. Their phylogenetic profiles and occurrence patterns are not linked to ANME-1b populations, indicating that electron donors other than methane, perhaps petroleum-derived hydrocarbons, drive sulfate reduction. The archaeal component of anaerobic oxidation of methane is comprised of an active population of mainly ANME-1b in this hypersaline sediment.

SUBMITTER: Lloyd KG

PROVIDER: S-EPMC1636178 | biostudies-literature | 2006 Nov

REPOSITORIES: biostudies-literature

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An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments.

Lloyd Karen G KG Lapham Laura L Teske Andreas A

Applied and environmental microbiology 20060915 11

Sediments overlying a brine pool methane seep in the Gulf of Mexico (Green Canyon 205) were analyzed using molecular and geochemical approaches to identify geochemical controls on microbial community composition and stratification. 16S rRNA gene and rRNA clone libraries, as well as mcrA gene clone libraries, showed that the archaeal community consists predominantly of ANME-1b methane oxidizers; no archaea of other ANME subgroups were found with general and group-specific PCR primers. The ANME-1b ...[more]

PMID: 16980428

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Project description:Marine sediments are important methane reservoirs. Methane efflux from the seabed is significantly restricted by anaerobic methanotrophic (ANME) archaea through a process known as anaerobic oxidation of methane (AOM). Different clades of ANME archaea occupy distinct niches in methane seeps, but their underlying molecular mechanisms still need to be fully understood. To provide genetic explanations for the niche partitioning of ANME archaea, we applied comparative genomic analysis to ANME archaeal genomes retrieved from global methane seeps. Our results showed that ANME-2 archaea are more prevalent than ANME-1 archaea in shallow sediments because they carry genes that encode a significantly higher number of outer membrane multiheme c-type cytochromes and flagellar proteins. These features make ANME-2 archaea perform direct interspecies electron transfer better and benefit more from electron acceptors in AOM. Besides, ANME-2 archaea carry genes that encode extra peroxidase compared to ANME-1 archaea, which may lead to ANME-2 archaea better tolerating oxygen toxicity. In contrast, ANME-1 archaea are more competitive in deep layers than ANME-2 archaea because they carry extra genes (mtb and mtt) for methylotrophic methanogenesis and a significantly higher number of frh and mvh genes for hydrogenotrophic methanogenesis. Additionally, ANME-1 archaea carry exclusive genes (sqr, TST, and mddA) involved in sulfide detoxification compared to ANME-2 archaea, leading to stronger sulfide tolerance. Overall, this study reveals the genomic mechanisms shaping the niche partitioning among ANME archaea in global methane seeps. IMPORTANCE Anaerobic methanotrophic (ANME) archaea are important methanotrophs in marine sediment, controlling the flux of biologically generated methane, which plays an essential role in the marine carbon cycle and climate change. So far, no strain of this lineage has been isolated in pure culture, which makes metagenomics one of the fundamental approaches to reveal their metabolic potential. Although the niche partitioning of ANME archaea was frequently reported in different studies, whether this pattern was consistent in global methane seeps had yet to be verified, and little was known about the genetic mechanisms underlying it. Here, we reviewed and analyzed the community structure of ANME archaea in global methane seeps and indicated that the niche partitioning of ANME archaea was statistically supported. Our comparative genomic analysis indicated that the capabilities of interspecies electron transfer, methanogenesis, and the resistance of oxygen and hydrogen sulfide could be critical in defining the distribution of ANME archaea in methane seep sediment.

Project description: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. 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.IMPORTANCE Methane oxidation in anaerobic environments can be accomplished by a number of archaeal groups, some of which live in syntrophic relationships with bacteria in structured consortia. Little is known of the distinguishing characteristics of these groups. Here, we applied imaging approaches to better understand the properties of these cells. We found unexpected morphological, structural, and volume variability of these uncultured groups by correlating fluorescence labeling of cells with electron microscopy observables.

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An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments.

Publications

An anaerobic methane-oxidizing community of ANME-1b archaea in hypersaline Gulf of Mexico sediments.

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