The discovery of archaeal lineages is critical to our understanding of the universal tree of life and evolutionary history of the Earth. Geochemically diverse thermal environments in Yellowstone National Park provide unprecedented opportunities for studying archaea in habitats that may represent analogues of early Earth. Here, we report the discovery and characterization of a phylum-level archaeal lineage proposed and herein referred to as the ‘Marsarchaeota’, after the red planet. The Marsarchaeota contains at least two major subgroups prevalent in acidic, microaerobic geothermal Fe(III) oxide microbial mats across a temperature range from ~50–80 °C. Metagenomics, single-cell sequencing, enrichment culturing and in situ transcriptional analyses reveal their biogeochemical role as facultative aerobic chemoorganotrophs that may also mediate the reduction of Fe(III). Phylogenomic analyses of replicate assemblies corresponding to two groups of Marsarchaeota indicate that they branch between the Crenarchaeota and all other major archaeal lineages. Transcriptomic analyses of several Fe(III) oxide mat communities reveal that these organisms were actively transcribing two different terminal oxidase complexes in situ and genes comprising an F420-dependent butanal catabolism. The broad distribution of Marsarchaeota in geothermal, microaerobic Fe(III) oxide mats suggests that similar habitat types probably played an important role in the evolution of archaea.
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The authors acknowledge support from the DOE Pacific Northwest National Laboratory (subcontracts 112443 and 254840), DOE Joint Genome Institute Community Sequencing Program (CSP 787081 and CSP 701), National Science Foundation Integrative Graduate Education and Research Traineeship Program (Z.J.J. and J.P.B.) (NSF DGE 0654336) and Montana Agricultural Experiment Station (W.P.I.). Work conducted by the Pacific Northwest National Laboratory (Foundational Scientific Focus Area) and Joint Genome Institute (DOE-AC02-05CH11231) is supported by the Genomic Science Program, Office of Biological and Environmental Research, US DOE. The authors appreciate assistance from S. Tringe, T. Woyke and D. Goudeau for genome and single-cell sequencing at the DOE Joint Genome Institute, C. Carey and A. Mazurie (MSU) for Illumina metagenome and iTag data processing, R. Jennings (MSU) for genome curation, R. Carlson (MSU) for collaboration on metabolic pathway analysis, and C. Hendrix, S. Sigler and D. Hallac (Center for Resources, YNP) for permitting this work in YNP (permits YELL-SCI-5068 and -5686). Computations were performed on the Hyalite High-Performance Computing System, operated and supported by MSU’s Information Technology Center.
The authors declare no competing interests.
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Supplementary Figures 1–12, Supplementary References.
List of different species of either Archaea, Bacteria or Eukarya and 55 proteins used in phylogenomic analyses (this is essentially the same group of proteins).
Metagenomes (M), transcriptomes (T) and single amplified genomes (SAG) of high-temperature, acidic iron oxide microbial mats from Yellowstone National Park that have been used in the study and description of Marsarchaeota groups 1 and 2. Sequence assemblies are available on IMG/M (DOE-Joint Genome Institute, Walnut Creek, CA).
Transcriptome reads mapped to annotated genome sequence of Marsarchaeota group 1 (sheet MarsG1-r04) and group 2 (sheet MarsG2-r02) for three Fe(III) oxide microbial mats (RPKM values) from Norris Geyser Basin (YNP).
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