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Diversity of methane-cycling archaea in hydrothermal sediment investigated by general and group-specific PCR primers.

ABSTRACT: The zonation of anaerobic methane-cycling Archaea in hydrothermal sediment of Guaymas Basin was studied by general primerpairs (mcrI, ME1/ME2, mcrIRD) targeting the alpha subunit of methyl coenzyme M reductase gene (mcrA) and by new group specific mcrA and 16S rRNA gene primer pairs. The mcrIRD primer pair outperformed the other general mcrA primer pairs indetection sensitivity and phylogenetic coverage. Methanotrophic ANME-1 Archaea were the only group detected with group specific primers only. The detection of 14 mcrA lineages surpasses the diversity previously found in this location. Most phylotypes have high sequence similarities to hydrogenotrophs, methylotrophs, and anaerobic methanotrophs previously detected at Guaymas Basin or at hydrothermal vents, cold seeps, and oil reservoirs worldwide. Additionally, five mcrA phylotypes belonging to newly defined lineages are detected. Two of these belong to deeply branching new orders, while the others are new species or genera of Methanopyraceae and Methermicoccaceae. Downcore diversity decreases from all groups detected in the upper 6 cm(2 to 40 °C, sulfate measurable to 4 cm) to only two groups below 6 cm (>40 °C). Despite the presence of hyperthermophilic genera (Methanopyrus, Methanocaldococcus) in cooler surface strata, no genes were detected below 10 cm (>60 °C). While mcrAbased and 16S rRNA gene-based community compositions are generally congruent, the deeply branching mcrA cannot be assigned to specific 16S rRNA gene lineages. Our study indicates that even among well-studied metabolic groups and in previously characterized model environments, major evolutionary branches are overlooked. Detecting these groups by improved molecular biological methods is a crucial first step toward understanding their roles in nature.

SUBMITTER: Lever MA

PROVIDER: S-EPMC4309701 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Diversity of methane-cycling archaea in hydrothermal sediment investigated by general and group-specific PCR primers.

Lever Mark A MA Teske Andreas P AP

Applied and environmental microbiology 20150201 4

The zonation of anaerobic methane-cycling Archaea in hydrothermal sediment of Guaymas Basin was studied by general primerpairs (mcrI, ME1/ME2, mcrIRD) targeting the alpha subunit of methyl coenzyme M reductase gene (mcrA) and by new group specific mcrA and 16S rRNA gene primer pairs. The mcrIRD primer pair outperformed the other general mcrA primer pairs indetection sensitivity and phylogenetic coverage. Methanotrophic ANME-1 Archaea were the only group detected with group specific primers only. ...[more]

PMID: 25527539

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Project description:Hydrothermal vents release reduced compounds and small organic carbon compounds into the surrounding seawater, providing essential substrates for microbial growth and bioenergy transformations. Despite the wide distribution of the marine benthic group E archaea (referred to as Hydrothermarchaeota) in the hydrothermal environment, little is known about their genomic repertoires and biogeochemical significance. Here, we studied four highly complete (>80%) metagenome-assembled genomes (MAGs) from a black smoker chimney and the surrounding sulfur-rich sediments on the South Atlantic Mid-Ocean Ridge and publicly available data sets (the Integrated Microbial Genomes system of the U.S. Department of Energy-Joint Genome Institute and NCBI SRA data sets). Genomic analysis suggested a wide carbon metabolic diversity of Hydrothermarchaeota members, including the utilization of proteins, lactate, and acetate; the anaerobic degradation of aromatics; the oxidation of C1 compounds (CO, formate, and formaldehyde); the utilization of methyl compounds; CO2 incorporation by the tetrahydromethanopterin-based Wood-Ljungdahl pathway; and participation in the type III ribulose-1,5-bisphosphate carboxylase/oxygenase-based Calvin-Benson-Bassham cycle. These microbes also potentially oxidize sulfur, arsenic, and hydrogen and engage in anaerobic respiration based on sulfate reduction and denitrification. Among the 140 MAGs reconstructed from the black smoker chimney microbial community (including Hydrothermarchaeota MAGs), community-level metabolic predictions suggested a redundancy of carbon utilization and element cycling functions and interactive syntrophic and sequential utilization of substrates. These processes might make various carbon and energy sources widely accessible to the microorganisms. Further, the analysis suggested that Hydrothermarchaeota members contained important functional components obtained from the community via lateral gene transfer, becoming a distinctive clade. This might serve as a niche-adaptive strategy for metabolizing heavy metals, C1 compounds, and reduced sulfur compounds. Collectively, the analysis provides comprehensive metabolic insights into the Hydrothermarchaeota IMPORTANCE This study provides comprehensive metabolic insights into the Hydrothermarchaeota from comparative genomics, evolution, and community-level perspectives. Members of the Hydrothermarchaeota synergistically participate in a wide range of carbon-utilizing and element cycling processes with other microorganisms in the community. We expand the current understanding of community interactions within the hydrothermal sediment and chimney, suggesting that microbial interactions based on sequential substrate metabolism are essential to nutrient and element cycling.

Dataset Information

Diversity of methane-cycling archaea in hydrothermal sediment investigated by general and group-specific PCR primers.

Publications

Diversity of methane-cycling archaea in hydrothermal sediment investigated by general and group-specific PCR primers.

Similar Datasets

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