Ammonia-oxidizing archaea are ubiquitous in marine and terrestrial environments and now thought to be significant contributors to carbon and nitrogen cycling. The isolation of Candidatus “ Nitrosopumilus maritimus ” strain SCM1 provided the opportunity for linking its chemolithotrophic physiology with a genomic inventory of the globally distributed archaea. Here we report the 1,645,259-bp closed genome of strain SCM1, revealing highly copper-dependent systems for ammonia oxidation and electron transport that are distinctly different from known ammonia-oxidizing bacteria. Consistent with in situ isotopic studies of marine archaea, the genome sequence indicates N. maritimus grows autotrophically using a variant of the 3-hydroxypropionate/4-hydroxybutryrate pathway for carbon assimilation, while maintaining limited capacity for assimilation of organic carbon. This unique instance of archaeal biosynthesis of the osmoprotectant ectoine and an unprecedented enrichment of multicopper oxidases, thioredoxin-like proteins, and transcriptional regulators points to an organism responsive to environmental cues and adapted to handling reactive copper and nitrogen species that likely derive from its distinctive biochemistry. The conservation of N. maritimus gene content and organization within marine metagenomes indicates that the unique physiology of these specialized oligophiles may play a significant role in the biogeochemical cycles of carbon and nitrogen.
Although anoxygenic photosynthesis is thought to play an important role in the primary productivity of permanently frozen lakes in the Antarctic dry valleys, the bacterial communities responsible for this metabolism remain uncharacterized. Here we report the composition and activity of phototrophic purple bacteria in Lake Fryxell, Antarctica, as determined by analysis of a photosynthesis-specific gene, pufM. The results revealed an extensive diversity and highly stratified distribution of purple nonsulfur bacteria in Lake Fryxell and showed which phylotypes produced pufM transcripts in situ. Enrichment cultures for purple bacteria yielded two morphotypes, each with a pufM signature identical to signatures detected by environmental screening. The isolates also contained gas vesicles, buoyancy structures previously unknown in purple nonsulfur bacteria, that may be necessary for these organisms to position themselves at specific depths within the nearly freezing water column.Lake Fryxell is a meromictic lake located 18 m above sea level at the entrance of Taylor Valley adjacent to McMurdo Sound, Antarctica (17). The lake is a closed basin with a maximum depth of 19 m (28). Lake Fryxell has undergone several dry-down periods in the past, resulting in slightly saline bottom waters overlaid with more dilute water introduced from glacial meltwater streams (12,20). This process has resulted in a gradient of solutes in the water column that is further stabilized by a perennial ice cover that is 3 to 5 m thick (25,28). The mixolimnion of the water column is supersaturated with oxygen, while the monimolimnion is anoxic due to limited gas exchange imposed by the perennial ice cover. The latter also serves as a barrier to light penetration, allowing only a small amount of light to reach the water column; for example, in Lake Fryxell, photosynthetically active radiation (PAR) is reduced by more than 90% from a depth of 4 to 9 m and by another 90% from 9 to 11 m (2, 23).There have been extensive studies of the geochemistry of Lake Fryxell, but to date only a few studies of the microbial communities that inhabit the lake have been reported (16,24). These studies focused on ammonia-oxidizing bacteria (members of the ␥ and  subdivisions of the Proteobacteria) within the water column and the contributions of cyanobacteria inhabiting the lake's ice cover to primary production in the dry valley ecosystem (6, 29). Studies of the bacterial diversity of microbial mat samples collected from moats that surround the lake during the austral summer season showed a large degree of microbial diversity, including both gram-positive and gramnegative bacteria, as well as Archaea (4).The presence of a year-round ice layer on Lake Fryxell prevents active mixing and maintains an extensive anoxic zone containing sulfide, which is suitable for development of anoxygenic phototrophic purple bacteria (21, 23). These organisms, although phototrophic, do not evolve oxygen and are members of the ␣, , and ␥ subdivisions of the Proteobacteria (10, 11). The...
The permanently frozen freshwater Lake Fryxell, located in the Dry Valleys of Antarctica, exhibits an ideal geochemistry for microbial sulfate reduction. To investigate the population of sulfate-reducing bacteria in Lake Fryxell, both 16S rRNA gene and metabolic primer sets targeting the dsrA gene for the dissimilatory sulfite reductase alpha subunit were employed to analyze environmental DNA obtained from the water column and sediments of Lake Fryxell. In addition, enrichment cultures of sulfate-reducing bacteria established at 4°C from Lake Fryxell water were also screened using the dsrA primer set. The sequence information obtained showed that a diverse group of sulfate-reducing prokaryotes of the domain Bacteria inhabit Lake Fryxell. With one exception, the enrichment culture sequences were not represented within the environmental sequences. Sequence data were compared with the geochemical profile of Lake Fryxell to identify possible connections between the diversity of sulfate-reducing bacteria and limnological conditions. Several clone groups were highly localized with respect to lake depth and, therefore, experienced specific physiochemical conditions. However, all sulfate-reducing bacteria inhabiting Lake Fryxell must function under the constantly cold conditions characteristic of this extreme environment.
Archaea were detected in molecular diversity studies of the permanently frozen Lake Fryxell, Antarctica. Two clusters of methanogens were detected in the sediments, and another cluster of possibly methanotrophic Euryarchaeota was detected in the anoxic water column just above the sediments. One crenarchaeote was detected in water just below the oxycline. The Archaea present in Lake Fryxell are likely involved in the major biogeochemical cycles that occur there.
Methanogens represent some of the most oxygen-sensitive organisms in laboratory culture. Recent studies indicate that they have developed mechanisms to deal with brief oxygen exposure. MsvR is a transcriptional regulator that has a domain architecture unique to a select group of methanogens. Here, runoff in vitro transcription assays were used to demonstrate that MsvR regulates transcription of the divergently transcribed fpaA-rlp-rub operon in Methanothermobacter thermautotrophicus in addition to transcription from its own promoter. The protein products of the fpaA-rlp-rub operon have previously been implicated in oxidative stress responses in M. thermautotrophicus. Additionally, electrophoretic mobility shift assays (EMSAs) and DNase I footprinting were used to confirm a binding site inferred by bioinformatic analysis. Sequence mutations within these binding sites did not significantly alter EMSA shifting patterns on longer templates but did on shorter 50-bp fragments encompassing only the region containing the binding sites. Footprinting confirmed that the regions protected for the longer mutant templates are at different positions within the intergenic region compared to those seen in the intact intergenic region. Oxidized and reduced preparations of MsvR demonstrated different EMSA binding patterns and regions of protection on the intergenic sequence, suggesting that MsvR may play a role in detecting the redox state of the cell.Biological methane production is limited to a small group of microorganisms in the domain Archaea that are termed methanogens. These organisms are strict anaerobes that can generate methane from H 2 and CO 2 and/or a limited series of C 1 compounds, depending upon the organism (5). Despite a necessity for growth in environments devoid of oxygen, the genomes of methanogens encode various enzymes (e.g., superoxide dismutase and alkyl hydroperoxide reductase) involved in the detoxification of reactive oxygen species. Previous studies have shown peroxide stress has little effect on methane production and overall growth yield in the hydrogenotrophic methanogen Methanothermobacter thermautotrophicus. The same study identified upregulation of the fpaA-rlp-rub operon (mth1350 to mth1352) believed to be involved in the detoxification of reactive oxygen species (10). This operon encodes a flavoprotein (fpaA), a rubrerythrin-like protein (rlp), and a rubredoxin (rub) (10,19). A homologue of the flavoprotein from the methanogen Methanobrevibacter arboriphilus has been demonstrated to reduce O 2 in the presence of H 2 and was reclassified as an F 420 H 2 oxidase (24). This lends further evidence to support the role of proteins encoded by this operon in the detoxification of reactive oxygen species.The archaeal transcription machinery represents a chimeric system with components reminiscent of features found in the other two domains of life, Bacteria and Eukarya. The multisubunit RNA polymerase is similar to the eukaryotic RNA polymerase II complex and, as is the case for the eukaryotic system, is...
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