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Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats

Nature Microbiology volume 3, pages 732–740 (2018)Cite this article

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Abstract

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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Fig. 1: Phylogenomic analysis of the candidate phylum Marsarchaeota (groups 1 and 2).
Fig. 2: Genome-identity correlation matrix of Marsarchaeota groups 1 and 2 compared with representatives of major archaeal lineages (top : average amino acid identity; bottom: average nucleotide identity).
Fig. 3: Scanning electron micrographs (SEM) of group 2 Marsarchaeota.
Fig. 4: Metatranscriptomic analysis.

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Acknowledgements

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.

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Author notes

  1. Zackary J. Jay

    Present address: Department of Chemical and Biological Engineering and Center for Biofilm Engineering, Montana State University, Bozeman, MT, USA

  2. Jacob P. Beam

    Present address: Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA

  3. Mark A. Kozubal

    Present address: Sustainable Bioproducts, Bozeman, MT, USA

  4. These authors contributed equally: Zackary J. Jay, Jacob P. Beam.

Authors and Affiliations

  1. Thermal Biology Institute and Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, USA

    Zackary J. Jay, Jacob P. Beam, Mark A. Kozubal & William P. Inskeep

  2. Department of Microbiology and Immunology, Montana State University, Bozeman, MT, USA

    Mensur Dlakić

  3. Center for Bioinformatics, Indiana University, Bloomington, IN, USA

    Douglas B. Rusch

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Contributions

W.P.I., Z.J.J., J.P.B. and M.A.K. designed the study. Z.J.J., J.P.B., M.A.K. and W.P.I. collected and analysed the field data. Z.J.J., M.D. and D.B.R. conducted the informatic analyses. M.D., W.P.I. and J.P.B. conducted the phylogenetic analysis. M.A.K. and J.P.B. established and analysed the enrichment cultures. Z.J.J. and J.P.B analysed the transcriptomic data. J.P.B. and W.P.I. performed microscopy and FISH analysis. W.P.I., M.D., Z.J.J. and J.P.B. wrote the manuscript. All authors reviewed and edited the manuscript.

Corresponding author

Correspondence to William P. Inskeep.

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Supplementary information

Supplementary Information

Supplementary Figures 1–12, Supplementary References.

Reporting Summary

Supplementary Table 1

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).

Supplementary Table 2

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).

Supplementary Table 4

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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Jay, Z.J., Beam, J.P., Dlakić, M. et al. Marsarchaeota are an aerobic archaeal lineage abundant in geothermal iron oxide microbial mats. Nat Microbiol 3, 732–740 (2018). https://doi.org/10.1038/s41564-018-0163-1

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