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Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw

Abstract

Permafrost contains an estimated 1672 Pg carbon (C), an amount roughly equivalent to the total currently contained within land plants and the atmosphere1,2,3. This reservoir of C is vulnerable to decomposition as rising global temperatures cause the permafrost to thaw2. During thaw, trapped organic matter may become more accessible for microbial degradation and result in greenhouse gas emissions4,5. Despite recent advances in the use of molecular tools to study permafrost microbial communities6,7,8,9, their response to thaw remains unclear. Here we use deep metagenomic sequencing to determine the impact of thaw on microbial phylogenetic and functional genes, and relate these data to measurements of methane emissions. Metagenomics, the direct sequencing of DNA from the environment, allows the examination of whole biochemical pathways and associated processes, as opposed to individual pieces of the metabolic puzzle. Our metagenome analyses reveal that during transition from a frozen to a thawed state there are rapid shifts in many microbial, phylogenetic and functional gene abundances and pathways. After one week of incubation at 5 °C, permafrost metagenomes converge to be more similar to each other than while they are frozen. We find that multiple genes involved in cycling of C and nitrogen shift rapidly during thaw. We also construct the first draft genome from a complex soil metagenome, which corresponds to a novel methanogen. Methane previously accumulated in permafrost is released during thaw and subsequently consumed by methanotrophic bacteria. Together these data point towards the importance of rapid cycling of methane and nitrogen in thawing permafrost.

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Figure 1: Bacterial oxidation of trapped CH 4 released from Hess Creek permafrost after thaw.
Figure 2: Draft methanogen genome assembly.
Figure 3: Thaw-induced shifts of phylogenetic and functional genes in metagenomes.
Figure 4: Conceptual model of C and N cycling in Arctic soils based on metagenome data.

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Acknowledgements

The work conducted by the Lawrence Berkeley National Laboratory Earth Sciences Division (Laboratory Directed Research Development) and the Joint Genome Institute was supported in part by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. This study was also supported by the Venture Capital and Yukon River Basin project of the United States Geological Survey. We acknowledge the technical support by the Joint Genome Institute production team. We thank A. Sczyrba, R. Egan and S. Canon for discussions and advice.

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Authors and Affiliations

Authors

Contributions

J.K.J., M.P.W. and K.M.D. conceived the incubation experiments. M.P.W. collected the samples. M.P.W. and S.J.B. conducted the incubation experiments. R.M., K.L.C. and K.M.D. performed the DNA extractions. R.M. created the shotgun sequencing libraries and conducted bioinformatics analyses. R.M. and K.M.D. performed statistical analyses. R.M. and M.M.D. performed qPCR experiments. R.M. and J.K.J. wrote the paper. All authors discussed the results and commented on the manuscript. E.M.R. M.P.W. and J.K.J. obtained funding for the study.

Corresponding author

Correspondence to Janet K. Jansson.

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The authors declare no competing financial interests.

Additional information

All annotated assembled sequences were incorporated into the IMG/M system with the Taxon Object ID 2067725009. Raw Illumina and 454 pyrotag sequence reads and a list containing the subset of contigs belonging to the draft methanogen genome are available at https://www.jgi.doe.gov/downloads/Permafrost_metagenome.

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The file contains Supplementary Figures 1-16 with legends, Supplementary Tables 1-7 and additional references. (PDF 4748 kb)

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Mackelprang, R., Waldrop, M., DeAngelis, K. et al. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368–371 (2011). https://doi.org/10.1038/nature10576

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