Identification of the dominant sulfate‐reducing bacterial partner of anaerobic methanotrophs of the ANME‐2 clade

Schreiber, Lars; Holler, Thomas; Knittel, Katrin; Meyerdierks, Anke; Amann, Rudolf

doi:10.1111/j.1462-2920.2010.02275.x

Cited by 160 publications

(180 citation statements)

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“…However, the presently obtained AOM enrichment characterized by a high proportion of related 16S rRNA genes did not show detectable sulfate reduction activity with butane instead of methane within an incubation time of 7 weeks. Corresponding to the naming of bacterial seep clusters identified at cold seeps ('Seep-SRB-1 to -4' and subgroups; Knittel et al, 2003;Schreiber et al, 2010), we named this new group of thermophilic, ANME-associated bacteria 'HotSeep-1'.…”

Section: Thermophilic Anaerobic Methanotrophy T Holler Et Almentioning

confidence: 99%

“…Another group, ANME-3, occurs for instance at Haakon Mosby Mud Volcano (Niemann et al, 2006; in situ temperature À1.5 1C) and the Eastern Mediterranean seepages (Omoregie et al, 2008;14 1C). Cells of both groups form dense consortia with specific bacterial phylotypes clustering with sulfate-reducing Deltaproteobacteria (most often within Desulfosarcinales, Seep-SRB-1a; Schreiber et al, 2010) or relatives of Desulfobulbus Lösekann et al, 2007;Pernthaler et al, 2008;Schreiber et al, 2010), respectively. A third phylogenetic group, ANME-1, is dominant in the microbial mats covering chimney structures at methane seeps in the Black Sea (Michaelis et al, 2002; in situ temperature of B10 1C), and in several diffusive methane interfaces (Thomsen et al, 2001;Lanoil et al, 2005;Harrison et al, 2009;Aquilina et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Thermophilic anaerobic oxidation of methane by marine microbial consortia

Holler

Widdel

Knittel

et al. 2011

ISME J

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The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. AOM is performed by microbial consortia of archaea (ANME) associated with partners related to sulfate-reducing bacteria. In vitro enrichments of AOM were so far only successful at temperatures p25 1C; however, energy gain for growth by AOM with sulfate is in principle also possible at higher temperatures. Sequences of 16S rRNA genes and core lipids characteristic for ANME as well as hints of in situ AOM activity were indeed reported for geothermally heated marine environments, yet no direct evidence for thermophilic growth of marine ANME consortia was obtained to date. To study possible thermophilic AOM, we investigated hydrothermally influenced sediment from the Guaymas Basin. In vitro incubations showed activity of sulfate-dependent methane oxidation between 5 and 70 1C with an apparent optimum between 45 and 60 1C. AOM was absent at temperatures X75 1C. Long-term enrichment of AOM was fastest at 50 1C, yielding a 13-fold increase of methane-dependent sulfate reduction within 250 days, equivalent to an apparent doubling time of 68 days. The enrichments were dominated by novel ANME-1 consortia, mostly associated with bacterial partners of the deltaproteobacterial HotSeep-1 cluster, a deeply branching phylogenetic group previously found in a butane-amended 60 1C-enrichment culture of Guaymas sediments. The closest relatives (Desulfurella spp.; Hippea maritima) are moderately thermophilic sulfur reducers. Results indicate that AOM and ANME archaea could be of biogeochemical relevance not only in cold to moderate but also in hot marine habitats.

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Section: Thermophilic Anaerobic Methanotrophy T Holler Et Almentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Thermophilic anaerobic oxidation of methane by marine microbial consortia

Holler

Widdel

Knittel

et al. 2011

ISME J

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174

223

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“…In contrast, the cool sediment core is dominated by Thermodesulfobacteria, Betaproteobacteria and Gammaproteobacteria (Figure 5a). All sites contain Deltaproteobacteria; within this subphylum, the Desulfobacteriales include the sulfate-reducing syntrophs that physically associate with ANME archaea (Schreiber et al, 2010) (Figure 5a). Figure 5 Bar charts of V6 tagged sequencing for (a) bacterial and (b) archaeal primer sets, for the hot, warm and cool sediment samples (cores 4489,10-12 cm; core 4486-22, 6-8 cm; and core 4483-21, 8-10 cm, respectively).…”

Section: V6-tag Sequencingmentioning

confidence: 99%

Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments

et al. 2011

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Anaerobic oxidation of methane (AOM) was investigated in hydrothermal sediments of Guaymas Basin based on d 13 C signatures of CH 4 , dissolved inorganic carbon and porewater concentration profiles of CH 4 and sulfate. Cool, warm and hot in-situ temperature regimes (15-20 1C, 30-35 1C and 70-95 1C) were selected from hydrothermal locations in Guaymas Basin to compare AOM geochemistry and 16S ribosomal RNA (rRNA), mcrA and dsrAB genes of the microbial communities. 16S rRNA gene clone libraries from the cool and hot AOM cores yielded similar archaeal types such as Miscellaneous Crenarchaeotal Group, Thermoproteales and anaerobic methane-oxidizing archaea (ANME)-1; some of the ANME-1 archaea formed a separate 16S rRNA lineage that at present seems to be limited to Guaymas Basin. Congruent results were obtained by mcrA gene analysis. The warm AOM core, chemically distinct by lower porewater sulfide concentrations, hosted a different archaeal community dominated by the two deep subsurface archaeal lineages Marine Benthic Group D and Marine Benthic Group B, and by members of the Methanosarcinales including ANME-2 archaea. This distinct composition of the methane-cycling archaeal community in the warm AOM core was confirmed by mcrA gene analysis. Functional genes of sulfate-reducing bacteria and archaea, dsrAB, showed more overlap between all cores, regardless of the core temperature. 16S rRNA gene clone libraries with Euryarchaeota-specific primers detected members of the Archaeoglobus clade in the cool and hot cores. A V6-tag high-throughput sequencing survey generally supported the clone library results while providing high-resolution detail on archaeal and bacterial community structure. These results indicate that AOM and the responsible archaeal communities persist over a wide temperature range.

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“…Its upward flux to the sediment-water interface is strongly reduced by sulfate-dependent anaerobic oxidation of methane (AOM) (1,2). AOM is performed by syntrophic associations of anaerobic methane-oxidizing archaea (ANMEs) (3,4) and their sulfate-reducing bacterial partners (SRBs) (mainly relatives of Desulfosarcina or Desulfobulbus) (5)(6)(7)(8). The free energy yield of the AOM net reaction is one of the lowest known for catabolic reactions under environmental conditions (ΔG ranges from -20 to -40 kJ·mol -1 ; e.g., refs.…”

mentioning

confidence: 99%

Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities

Kellermann

Wegener

Elvert

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The methane-rich, hydrothermally heated sediments of the Guaymas Basin are inhabited by thermophilic microorganisms, including anaerobic methane-oxidizing archaea (mainly ANME-1) and sulfatereducing bacteria (e.g., HotSeep-1 cluster). We studied the microbial carbon flow in ANME-1/ HotSeep-1 enrichments in stable-isotopeprobing experiments with and without methane. The relative incorporation of 13 C from either dissolved inorganic carbon or methane into lipids revealed that methane-oxidizing archaea assimilated primarily inorganic carbon. This assimilation is strongly accelerated in the presence of methane. Experiments with simultaneous amendments of both 13 C-labeled dissolved inorganic carbon and deuterated water provided further insights into production rates of individual lipids derived from members of the methane-oxidizing community as well as their carbon sources used for lipid biosynthesis. In the presence of methane, all prominent lipids carried a dual isotopic signal indicative of their origin from primarily autotrophic microbes. In the absence of methane, archaeal lipid production ceased and bacterial lipid production dropped by 90%; the lipids produced by the residual fraction of the metabolically active bacterial community predominantly carried a heterotrophic signal. Collectively our results strongly suggest that the studied ANME-1 archaea oxidize methane but assimilate inorganic carbon and should thus be classified as methane-oxidizing chemoorganoautotrophs.methanotrophy | biomarker | acetyl-CoA pathway | syntrophy M ethane is an important greenhouse gas and the most abundant hydrocarbon in marine sediments. Its upward flux to the sediment-water interface is strongly reduced by sulfate-dependent anaerobic oxidation of methane (AOM) (1, 2). AOM is performed by syntrophic associations of anaerobic methane-oxidizing archaea (ANMEs) (3, 4) and their sulfate-reducing bacterial partners (SRBs) (mainly relatives of Desulfosarcina or Desulfobulbus) (5-8). The free energy yield of the AOM net reaction is one of the lowest known for catabolic reactions under environmental conditions (ΔG ranges from -20 to -40 kJ·mol -1 ; e.g., refs. 9, 10). Consequently, activity and biomass doubling times determined under optimized laboratory conditions range from 2 to 5 mo (11) and growth yields are extremely low, around 1% relative to oxidized methane (11,12). The biomass of ANMEs and SRBs involved in AOM is usually strongly depleted in 13 C. For instance, at methane seep locations, the δ 13 C values of specific bacterial fatty acids and archaeal ether lipids range from -60 to -100‰ and -70 to -130‰, respectively (e.g., refs. 13-17). Such low values have been interpreted as evidence for the incorporation of 13 C-depleted methane into biomass (e.g., refs. 3, 4, 18).One way to identify the carbon sources of microbial biomass is to perform stable-isotope-probing (SIP) experiments (19), followed by analysis of biomolecules such as membrane lipids (lipid-SIP hereafter). Application of lipid-SIP to cold seep sediments and micro...

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Identification of the dominant sulfate‐reducing bacterial partner of anaerobic methanotrophs of the ANME‐2 clade

Cited by 160 publications

References 60 publications

Thermophilic anaerobic oxidation of methane by marine microbial consortia

Thermophilic anaerobic oxidation of methane by marine microbial consortia

Anaerobic oxidation of methane at different temperature regimes in Guaymas Basin hydrothermal sediments

Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities

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