Abstract

Over 20% of Earth’s terrestrial surface is underlain by permafrost with vast stores of carbon that, once thawed, may represent the largest future transfer of carbon from the biosphere to the atmosphere1. This process is largely dependent on microbial responses, but we know little about microbial activity in intact, let alone in thawing, permafrost. Molecular approaches have recently revealed the identities and functional gene composition of microorganisms in some permafrost soils2,3,4 and a rapid shift in functional gene composition during short-term thaw experiments3. However, the fate of permafrost carbon depends on climatic, hydrological and microbial responses to thaw at decadal scales5,6. Here we use the combination of several molecular ‘omics’ approaches to determine the phylogenetic composition of the microbial communities, including several draft genomes of novel species, their functional potential and activity in soils representing different states of thaw: intact permafrost, seasonally thawed active layer and thermokarst bog. The multi-omics strategy reveals a good correlation of process rates to omics data for dominant processes, such as methanogenesis in the bog, as well as novel survival strategies for potentially active microbes in permafrost.

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Acknowledgements

We thank R. Hettich and the Organic and Biological Mass Spectrometry group at Oak Ridge National Laboratory for access to mass spectrometry instrumentation. M. Haw, K. Li, K. Chavarria and R. Lamendella are acknowledged for help with pre-processing frozen samples. We thank K. Billis for help with RNA sequence preprocessing. This work was partly supported by the Director, Office of Science, Office of Biological and Environmental Research, Climate and Environmental Science Division, of the US Department of Energy, Terrestrial Ecosystem Science-Scientific Focus Area (TES-SFA), through a Community Sequencing Project at the DOE Joint Genome Institute (JGI CSP - 152) and by a Lawrence Berkeley National Laboratory Laboratory Directed Research & Development (LDRD) grant, all under contract number DE-AC02-05CH11231; by the Pacific Northwest National Laboratory under contract number DE-AC05-76RL01830; and by the Danish National Research Foundation (CENPERM DNRF100). The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the US Department of Energy under contract number DE-AC02-05CH11231. Additional funding and considerable logistic support were provided by the Bonanza Creek Long-Term Ecological Research Program, which is jointly funded by National Science Foundation (DEB 1026415) and the US Department of Agriculture Forest Service, Pacific Northwest Research Station (PNW01-JV112619320-16). Support was also received from the US Geological Survey Climate R&D Program and Alaska Climate Science Center. J.Hu. was supported by Academy of Finland grant number 135669.

Author information

Author notes

    • Jenni Hultman
    • , Manesh B. Shah
    • , Kostas Mavrommatis
    •  & Janet K. Jansson

    Present addresses: Department of Food Safety and Environmental Health, Agnes Sjöbergin katu 2, University of Helsinki, Helsinki 00014, Finland (J.H.); Oak Ridge National Laboratory, Biosciences Division, Tennessee 37831, USA (M.B.S.); Celgene Corporation, 1500 Owens Street, San Francisco, California 94158-2335, USA (K.M.); Biological Sciences Division, Pacific Northwest National Laboratory, 902 Battelle Boulevard, Richland, Washington 99352, USA (J.K.J.).

Affiliations

  1. Earth Sciences Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, California, 94720, USA

    • Jenni Hultman
    • , Maude M. David
    •  & Janet K. Jansson
  2. US Geological Survey, 345 Middlefield Road, Menlo Park, California 94025, USA

    • Mark P. Waldrop
    • , Jack McFarland
    • , Steven J. Blazewicz
    •  & Jennifer Harden
  3. Biology Department, 18111 Nordhoff Street, California State University Northridge, Northridge, California 91330, USA

    • Rachel Mackelprang
  4. US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California 94598, USA

    • Rachel Mackelprang
    • , Kostas Mavrommatis
    •  & Janet K. Jansson
  5. Department of Integrative Biology, 50 Stone Road East, University of Guelph, Guelph, Ontario N1G 2W1, Canada

    • Merritt R. Turetsky
  6. US Geological Survey, Alaska Cooperative Fish and Wildlife Research Unit, 211A Irving I Building, University of Alaska Fairbanks, Fairbanks, Alaska 99775, USA

    • A. David McGuire
  7. Chemical Sciences Division, One Bethel Valley Road, Building 1059, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831-6420, USA

    • Manesh B. Shah
    •  & Nathan C. VerBerkmoes
  8. Graduate School of Genome Science and Technology, University of Tennessee and Oak Ridge National Laboratory, 2510 River Drive, Knoxville, Tennessee 37996, USA

    • Lang Ho Lee
  9. Department of Plant and Microbial Biology, 111 Koshland Hall, University of California, Berkeley, Berkeley, California 94720, USA

    • Janet K. Jansson
  10. Center for Permafrost Research (CENPERM), Department of Biology, Universitetsparken 15, University of Copenhagen, Copenhagen, DK-2100 Copenhagen, Denmark

    • Janet K. Jansson

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Contributions

J.K.J., M.P.W. and J.Hu. planned the study. M.P.W. and J.M. collected the samples and J.M. performed the chemical analyses. J.Ha., M.R.T. and A.D.M. performed the site characterization. M.B.S., N.C.V., M.M.D. and L.H.L. performed the proteomics. J.Hu., R.M., S.J.B. and K.M. analysed the sequence data. J.Hu., M.P.W. and J.K.J. wrote the paper with contributions from all authors. J.Hu., J.K.J., M.P.W. and R.M. made the figures.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Janet K. Jansson.

The 454 nucleotide sequences have been deposited in Sequence Read Archive under BioProject number PRJNA222786, metagenomes and metatranscriptomes in IMG/M under Study ID Gs0063124 MG-RAST under project number 11953 and proteomics data in the PRIDE partner repository under dataset identifier PXD001131.

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https://doi.org/10.1038/nature14238

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