Abstract
Novel lineages of the phylum Thaumarchaeota are endemic to thermal habitats, and may exhibit physiological capabilities that are not yet observed in members of this phylum. The primary goals of this study were to conduct detailed phylogenetic and functional analyses of metagenome sequence assemblies of two different thaumarchaeal populations found in high-temperature (65–72 °C), acidic (pH∼3) iron oxide and sulfur sediment environments of Yellowstone National Park (YNP). Metabolic reconstruction was coupled with detailed geochemical measurements of each geothermal habitat and reverse-transcriptase PCR to confirm the in situ activity of these populations. Phylogenetic analyses of ribosomal and housekeeping proteins place these archaea near the root of the thaumarchaeal branch. Metabolic reconstruction suggests that these populations are chemoorganotrophic and couple growth with the reduction of oxygen or nitrate in iron oxide habitats, or sulfur in hypoxic sulfur sediments. The iron oxide population has the potential for growth via the oxidation of sulfide to sulfate using a novel reverse sulfate reduction pathway. Possible carbon sources include aromatic compounds (for example, 4-hydroxyphenylacetate), complex carbohydrates (for example, starch), oligopeptides and amino acids. Both populations contain a type III ribulose bisphosphate carboxylase/oxygenase used for carbon dioxide fixation or adenosine monophosphate salvage. No evidence for the oxidation of ammonia was obtained from de novo sequence assemblies. Our results show that thermoacidophilic Thaumarchaeota from oxic iron mats and hypoxic sulfur sediments exhibit different respiratory machinery depending on the presence of oxygen versus sulfide, represent deeply rooted lineages within the phylum Thaumarchaeota and are endemic to numerous sites in YNP.
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Acknowledgements
We appreciate support from the NSF-Integrative Graduate Education and Research Training Program to JPB and ZJJ (DGE 0654336), DOE-Pacific Northwest National Laboratory-Foundational Science Focus Area in Biological Interactions (Subcontract 112443), Douglas B Rusch at Indiana University, Bloomington, IN for NWF-PCA support, Susannah G Tringe at the DOE-JGI (Community Sequencing Program, CSP-787081) for metagenome sequencing performed at Dragon Spring (45 Mb Sanger) and Beowulf Spring (60 Mb 454), the J Craig Venter Institute for early Sanger sequencing at Beowulf Spring (12 Mb Sanger) and Justin O’Dea for positive amoA gene controls. The authors also appreciate comments from three anonymous reviewers that improved the quality of the final manuscript.
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Beam, J., Jay, Z., Kozubal, M. et al. Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park. ISME J 8, 938–951 (2014). https://doi.org/10.1038/ismej.2013.193
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DOI: https://doi.org/10.1038/ismej.2013.193
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