Dataset Information

Active Anaerobic Archaeal Methanotrophs in Recently Emerged Cold Seeps of Northern South China Sea.

ABSTRACT: Cold seep ecosystems are developed from methane-rich fluids in organic rich continental slopes, which are the source of various dense microbial and faunal populations. Extensive studies have been conducted on microbial populations in this unique environment; most of them were based on DNA, which could not resolve the activity of extant organisms. In this study, RNA and DNA analyses were performed to evaluate the active archaeal and bacterial communities and their network correlations, particularly those participating in the methane cycle at three sites of newly developed cold seeps in the northern South China Sea (nSCS). The results showed that both archaeal and bacterial communities were significantly different at the RNA and DNA levels, revealing a higher abundance of methane-metabolizing archaea and sulfate-reducing bacteria in RNA sequencing libraries. Site ROV07-01, which exhibited extensive accumulation of deceased Calyptogena clam shells, was highly developed, and showed diverse and active anaerobic archaeal methanotrophs (ANME)-2a/b and sulfate-reducing bacteria from RNA libraries. Site ROV07-02, located near carbonate crusts with few clam shell debris, appeared to be poorly developed, less anaerobic and less active. Site ROV05-02, colonized by living Calyptogena clams, could likely be intermediary between ROV07-01 and ROV07-02, showing abundant ANME-2dI and sulfate-reducing bacteria in RNA libraries. The high-proportions of ANME-2dI, with respect to ANME-2dII in the site ROV07-01 was the first report from nSCS, which could be associated with recently developed cold seeps. Both ANME-2dI and ANME-2a/b showed close networked relationships with sulfate-reducing bacteria; however, they were not associated with the same microbial operational taxonomic units (OTUs). Based on the geochemical gradients and the megafaunal settlements as well as the niche specificities and syntrophic relationships, ANMEs appeared to change in community structure with the evolution of cold seeps, which may be associated with the heterogeneity of their geochemical processes. This study enriched our understanding of more active sulfate-dependent anaerobic oxidation of methane (AOM) in poorly developed and active cold seep sediments by contrasting DNA- and RNA-derived community structure and activity indicators.

SUBMITTER: Zhang T

PROVIDER: S-EPMC7772427 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Active Anaerobic Archaeal Methanotrophs in Recently Emerged Cold Seeps of Northern South China Sea.

Zhang Tingting T Xiao Xi X Chen Songze S Zhao Jing J Chen Zongheng Z Feng Junxi J Liang Qianyong Q Phelps Tommy J TJ Zhang Chuanlun C

Frontiers in microbiology 20201216

Cold seep ecosystems are developed from methane-rich fluids in organic rich continental slopes, which are the source of various dense microbial and faunal populations. Extensive studies have been conducted on microbial populations in this unique environment; most of them were based on DNA, which could not resolve the activity of extant organisms. In this study, RNA and DNA analyses were performed to evaluate the active archaeal and bacterial communities and their network correlations, particular ...[more]

PMID: 33391242

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Project description:Cold seeps, located along the Sonora Margin transform fault in the Guaymas Basin, were extensively explored during the 'BIG' cruise in June 2010. They present a seafloor mosaic pattern consisting of different faunal assemblages and microbial mats. To investigate this mostly unknown cold and hydrocarbon-rich environment, geochemical and microbiological surveys of the sediments underlying two microbial mats and a surrounding macrofaunal habitat were analyzed in detail. The geochemical measurements suggest biogenic methane production and local advective sulfate-rich fluxes in the sediments. The distributions of archaeal communities, particularly those involved in the methane cycle, were investigated at different depths (surface to 18 cm below the sea floor (cmbsf)) using complementary molecular approaches, such as Automated method of Ribosomal Intergenic Spacer Analysis (ARISA), 16S rRNA libraries, fluorescence in situ hybridization and quantitative polymerase chain reaction with new specific primer sets targeting methanogenic and anaerobic methanotrophic lineages. Molecular results indicate that metabolically active archaeal communities were dominated by known clades of anaerobic methane oxidizers (archaeal anaerobic methanotroph (ANME)-1, -2 and -3), including a novel 'ANME-2c Sonora' lineage. ANME-2c were found to be dominant, metabolically active and physically associated with syntrophic Bacteria in sulfate-rich shallow sediment layers. In contrast, ANME-1 were more prevalent in the deepest sediment samples and presented a versatile behavior in terms of syntrophic association, depending on the sulfate concentration. ANME-3 were concentrated in small aggregates without bacterial partners in a restricted sediment horizon below the first centimetres. These niche specificities and syntrophic behaviors, depending on biological surface assemblages and environmental availability of electron donors, acceptors and carbon substrates, suggest that ANME could support alternative metabolic pathways than syntrophic anaerobic oxidation of methane.

Project description:Acetyl-CoA synthetase (ACS) and acetate ligase (ACD) are widespread among microorganisms, including archaea, and play an important role in their carbon metabolism, although only a few of these enzymes have been characterized. Anaerobic methanotrophs (ANMEs) have been reported to convert methane anaerobically into CO2, polyhydroxyalkanoate, and acetate. Furthermore, it has been suggested that they might be able to use acetate for anabolism or aceticlastic methanogenesis. To better understand the potential acetate metabolism of ANMEs, we characterized an ACS from ANME-2a as well as an ACS and an ACD from ANME-2d. The conversion of acetate into acetyl-CoA (Vmax of 8.4 μmol mg-1 min-1 and Km of 0.7 mM acetate) by the monomeric 73.8-kDa ACS enzyme from ANME-2a was more favorable than the formation of acetate from acetyl-CoA (Vmax of 0.4 μmol mg-1 min-1 and Km of 0.2 mM acetyl-CoA). The monomeric 73.4-kDa ACS enzyme from ANME-2d had similar Vmax values for both directions (Vmax,acetate of 0.9 μmol mg-1 min-1 versus Vmax,acetyl-CoA of 0.3 μmol mg-1 min-1). The heterotetrameric ACD enzyme from ANME-2d was active solely in the acetate-producing direction. Batch incubations of an enrichment culture dominated by ANME-2d fed with 13C2-labeled acetate produced 3 μmol of [13C]methane in 7 days, suggesting that this anaerobic methanotroph might have the potential to reverse its metabolism and perform aceticlastic methanogenesis using ACS to activate acetate albeit at low rates (2 nmol g [dry weight]-1 min-1). Together, these results show that ANMEs may have the potential to use acetate for assimilation as well as to use part of the surplus acetate for methane production. IMPORTANCE Acetyl-CoA plays a key role in carbon metabolism and is found at the junction of many anabolic and catabolic reactions. This work describes the biochemical properties of ACS and ACD enzymes from ANME-2 archaea. This adds to our knowledge of archaeal ACS and ACD enzymes, only a few of which have been characterized to date. Furthermore, we validated the in situ activity of ACS in ANME-2d, showing the conversion of acetate into methane by an enrichment culture dominated by ANME-2d.

Project description:BackgroundNatural gas contains methane and the gaseous alkanes ethane, propane and butane, which collectively influence atmospheric chemistry and cause global warming. Methane-oxidising bacteria, methanotrophs, are crucial in mitigating emissions of methane as they oxidise most of the methane produced in soils and the subsurface before it reaches the atmosphere. Methanotrophs are usually obligate, i.e. grow only on methane and not on longer chain alkanes. Bacteria that grow on the other gaseous alkanes in natural gas such as propane have also been characterised, but they do not grow on methane. Recently, it was shown that the facultative methanotroph Methylocella silvestris grew on ethane and propane, other components of natural gas, in addition to methane. Therefore, we hypothesised that Methylocella may be prevalent at natural gas seeps and might play a major role in consuming all components of this potent greenhouse gas mixture before it is released to the atmosphere.ResultsEnvironments known to be exposed to biogenic methane emissions or thermogenic natural gas seeps were surveyed for methanotrophs. 16S rRNA gene amplicon sequencing revealed that Methylocella were the most abundant methanotrophs in natural gas seep environments. New Methylocella-specific molecular tools targeting mmoX (encoding the soluble methane monooxygenase) by PCR and Illumina amplicon sequencing were designed and used to investigate various sites. Functional gene-based assays confirmed that Methylocella were present in all of the natural gas seep sites tested here. This might be due to its ability to use methane and other short chain alkane components of natural gas. We also observed the abundance of Methylocella in other environments exposed to biogenic methane, suggesting that Methylocella has been overlooked in the past as previous ecological studies of methanotrophs often used pmoA (encoding the alpha subunit of particulate methane monooxygenase) as a marker gene.ConclusionNew biomolecular tools designed in this study have expanded our ability to detect, and our knowledge of the environmental distribution of Methylocella, a unique facultative methanotroph. This study has revealed that Methylocella are particularly abundant at natural gas seeps and may play a significant role in biogeochemical cycling of gaseous hydrocarbons.

Dataset Information

Active Anaerobic Archaeal Methanotrophs in Recently Emerged Cold Seeps of Northern South China Sea.

Publications

Active Anaerobic Archaeal Methanotrophs in Recently Emerged Cold Seeps of Northern South China Sea.

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