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Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes

Nature volume 521, pages 208–212 (2015)Cite this article

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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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Figure 1: Microbial phylogenetic composition in permafrost, active layer and thermokarst bog soils.
Figure 2: Average MT/MG ratios.
Figure 3: Relationships among MG, MT and MP for nitrogen cycling (circle), sulphur cycling (square) and methanogenesis (triangle) in permafrost (blue), active layer (green) and thermokarst bog soils (pink).
Figure 4: Visualization of proteins identified from metaproteomics data sets.

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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

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

    Present address: 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.).,

Authors and 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, 94025, California, USA

    Mark P. Waldrop, Jack McFarland, Steven J. Blazewicz & Jennifer Harden

  3. Biology Department, 18111 Nordhoff Street, California State University Northridge, Northridge, 91330, California, USA

    Rachel Mackelprang

  4. US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, 94598, California, 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, 99775, Alaska, 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. Department of Biology, Center for Permafrost Research (CENPERM), Universitetsparken 15, University of Copenhagen, Copenhagen, DK-2100 Copenhagen, Denmark,

    Janet K. Jansson

Authors
  1. Jenni Hultman
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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.

Corresponding author

Correspondence to Janet K. Jansson.

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Competing interests

The authors declare no competing financial interests.

Additional information

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.

Extended data figures and tables

Extended Data Figure 1 Comparison of multi-omics data between the three zones.

The triplots visually present selected functions in (a) metagenomes, (b) metatranscriptomes and (c) metaproteomes in the three studied zones (permafrost, active layer and thermokarst bog). The colours correspond to SEED subsystems categories in MG-RAST; in addition, the closer the symbol is to the node of the triplot, the more abundant the gene, transcript or protein is in that particular soil type. Functions in the centre are shared among all three sites, those on edges are shared between two zones and those on the nodes are unique to that site. Owing to the large number of shared functions between bog and active layer in the metatranscriptomes, these categories are specifically compared in d.

Extended Data Figure 2 Shared and unique genes, transcripts and proteins in the three zones.

The Venn diagrams for (a) metagenome, (b) metatranscriptome and (c) metaproteome data illustrate the shared and unique genes, transcripts and proteins in the three zones.

Extended Data Figure 3 Heatmap showing the 40 most abundant transporters found in the metatranscriptomes.

Extended Data Figure 4 Abundance of genes involved in sulphate reduction, nitrogen cycle, methanogenesis and methane oxidation.

The relative abundance of each gene is shown; error bars, s.d. The genes with protein matches in the metaproteome data are marked with a triangle.

Extended Data Figure 5 The 20 most abundant OTUs found in permafrost, active layer and thermokarst bog.

a, Bacterial OTUs; b, archaeal OTUs. A single Chloroflexi OTU constituted up to 15% of the OTUs in permafrost and a draft genome bin was obtained that corresponded to this OTU (Extended Data Table 1). The abundant archaeal OTUs were methanogens.

Extended Data Figure 6 Comparison of abundant KEGG orthologous groups found in all three omics approaches (MG, MT and MP) for each site.

Permafrost: restriction modification systems, PAS sensors, ABC transporters for oligopeptides and nucleic-acid synthesis. Active layer: chaperonins, dehydrogenases and transporters for branched-chain amino acids and sugars. Thermokarst bog: methyl coenzyme M reductase, glycerol kinase, nucleic-acid synthesis and ATPases.

Extended Data Table 1 Metagenomic bins produced from the metagenomes
Full size table
Extended Data Table 2 Number of OTUs from 454 sequencing and alpha diversity indices
Full size table

Supplementary information

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Supplementary Data

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Hultman, J., Waldrop, M., Mackelprang, R. et al. Multi-omics of permafrost, active layer and thermokarst bog soil microbiomes. Nature 521, 208–212 (2015). https://doi.org/10.1038/nature14238

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