Dataset Information

Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs.

ABSTRACT: Recent progress based on single-cell genomics and metagenomic investigations of archaea in a variety of extreme environments has led to significant advances in our understanding of the diversity, evolution, and metabolic potential of archaea, yet the vast majority of archaeal diversity remains undersampled. In this work, we coordinated single-cell genomics with metagenomics in order to construct a near-complete genome from a deeply branching uncultivated archaeal lineage sampled from Great Boiling Spring (GBS) in the U.S. Great Basin, Nevada. This taxon is distantly related (distinct families) to an archaeal genome, designated "Novel Archaeal Group 1" (NAG1), which was extracted from a metagenome recovered from an acidic iron spring in Yellowstone National Park (YNP). We compared the metabolic predictions of the NAG1 lineage to better understand how these archaea could inhabit such chemically distinct environments. Similar to the NAG1 population previously studied in YNP, the NAG1 population from GBS is predicted to utilize proteins as a primary carbon source, ferment simple carbon sources, and use oxygen as a terminal electron acceptor under oxic conditions. However, GBS NAG1 populations contained distinct genes involved in central carbon metabolism and electron transfer, including nitrite reductase, which could confer the ability to reduce nitrite under anaerobic conditions. Despite inhabiting chemically distinct environments with large variations in pH, GBS NAG1 populations shared many core genomic and metabolic features with the archaeon identified from YNP, yet were able to carve out a distinct niche at GBS.

SUBMITTER: Becraft ED

PROVIDER: S-EPMC5671600 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs.

Becraft Eric D ED Dodsworth Jeremy A JA Murugapiran Senthil K SK Thomas Scott C SC Ohlsson J Ingemar JI Stepanauskas Ramunas R Hedlund Brian P BP Swingley Wesley D WD

Frontiers in microbiology 20171031

Recent progress based on single-cell genomics and metagenomic investigations of archaea in a variety of extreme environments has led to significant advances in our understanding of the diversity, evolution, and metabolic potential of archaea, yet the vast majority of archaeal diversity remains undersampled. In this work, we coordinated single-cell genomics with metagenomics in order to construct a near-complete genome from a deeply branching uncultivated archaeal lineage sampled from Great Boili ...[more]

PMID: 29163388

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Project description:Despite the ubiquity of ammonium in geothermal environments and the thermodynamic favorability of aerobic ammonia oxidation, thermophilic ammonia-oxidizing microorganisms belonging to the crenarchaeota kingdom have only recently been described. In this study, we analyzed microbial mats and surface sediments from 21 hot spring samples (pH 3.4 to 9.0; temperature, 41 to 86 degrees C) from the United States, China, and Russia and obtained 846 putative archaeal ammonia monooxygenase large-subunit (amoA) gene and transcript sequences, representing a total of 41 amoA operational taxonomic units (OTUs) at 2% identity. The amoA gene sequences were highly diverse, yet they clustered within two major clades of archaeal amoA sequences known from water columns, sediments, and soils: clusters A and B. Eighty-four percent (711/846) of the sequences belonged to cluster A, which is typically found in water columns and sediments, whereas 16% (135/846) belonged to cluster B, which is typically found in soils and sediments. Although a few amoA OTUs were present in several geothermal regions, most were specific to a single region. In addition, cluster A amoA genes formed geographic groups, while cluster B sequences did not group geographically. With the exception of only one hot spring, principal-component analysis and UPGMA (unweighted-pair group method using average linkages) based on the UniFrac metric derived from cluster A grouped the springs by location, regardless of temperature or bulk water pH, suggesting that geography may play a role in structuring communities of putative ammonia-oxidizing archaea (AOA). The amoA genes were distinct from those of low-temperature environments; in particular, pair-wise comparisons between hot spring amoA genes and those from sympatric soils showed less than 85% sequence identity, underscoring the distinctness of hot spring archaeal communities from those of the surrounding soil system. Reverse transcription-PCR showed that amoA genes were transcribed in situ in one spring and the transcripts were closely related to the amoA genes amplified from the same spring. Our study demonstrates the global occurrence of putative archaeal amoA genes in a wide variety of terrestrial hot springs and suggests that geography may play an important role in selecting different assemblages of AOA.

Project description:Terrestrial hot springs harbor diverse microbial communities whose compositions are shaped by the wide-ranging physico-chemistries of individual springs. The effect of enormous physico-chemical differences on bacterial and archaeal distributions and population structures is little understood. We therefore analysed the prevalence and relative abundance of bacteria and archaea in the sediments (n = 76) of hot spring features, in the Taupō Volcanic Zone (New Zealand), spanning large differences in major anion water chemistry, pH (2.0-7.5), and temperature (17.5-92.9 °C). Community composition, based on 16S rRNA amplicon sequence variants (ASVs) was strongly influenced by both temperature and pH. However, certain lineages characterized diverse hot springs. At the domain level, bacteria and archaea shared broadly equivalent community abundances across physico-chemically diverse springs, despite slightly lower bacteria-to-archaea ratios and microbial 16S rRNA gene concentrations at higher temperatures. Communities were almost exclusively dominated by Proteobacteria, Euryarchaeota or Crenarchaeota. Eight archaeal and bacterial ASVs from Thermoplasmatales, Desulfurellaceae, Mesoaciditogaceae and Acidithiobacillaceae were unusually prevalent (present in 57.9-84.2% of samples) and abundant (1.7-12.0% sample relative abundance), and together comprised 44% of overall community abundance. Metagenomic analyses generated multiple populations associated with dominant ASVs, and showed characteristic traits of each lineage for sulfur, nitrogen and hydrogen metabolism. Differences in metabolic gene composition and genome-specific metabolism delineated populations from relatives. Genome coverage calculations showed that populations associated with each lineage were distributed across a physicochemically broad range of hot springs. Results imply that certain bacterial and archaeal lineages harbor different population structures and metabolic potentials for colonizing diverse hot spring environments.

Dataset Information

Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs.

Publications

Genomic Comparison of Two Family-Level Groups of the Uncultivated NAG1 Archaeal Lineage from Chemically and Geographically Disparate Hot Springs.

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