Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming
- aDepartment of Arctic and Marine Biology, University of Tromsø The Arctic University of Norway, 9037 Tromsø, Norway;
- bDepartment of Ecogenomics and Systems Biology, University of Vienna, 1090 Vienna, Austria;
- cAustrian Polar Research Institute, 1090, Vienna, Austria; and
- dDepartment of Biochemistry, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany
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Edited by Edward F. DeLong, University of Hawaii, Manoa, Honolulu, HI, and approved April 6, 2015 (received for review October 31, 2014)
Significance
Microorganisms are key players in emissions of the greenhouse gas (GHG) methane from anoxic carbon-rich peat soils of the Arctic permafrost region. Although available data and modeling suggest a significant temperature-induced increase of GHG emissions from these regions by the end of this century, the controls of and interactions within the underlying microbial networks are largely unknown. This temperature-gradient study of an Arctic peat soil using integrated omics techniques reveals critical temperatures at which microbial adaptations cause changes in metabolic bottlenecks of anaerobic carbon-degradation pathways. In particular taxonomic shifts within functional guilds at different levels of the carbon degradation cascade enable a fast adaptation of the microbial system resulting in high methane emissions at all temperatures.
Abstract
Arctic permafrost soils store large amounts of soil organic carbon (SOC) that could be released into the atmosphere as methane (CH4) in a future warmer climate. How warming affects the complex microbial network decomposing SOC is not understood. We studied CH4 production of Arctic peat soil microbiota in anoxic microcosms over a temperature gradient from 1 to 30 °C, combining metatranscriptomic, metagenomic, and targeted metabolic profiling. The CH4 production rate at 4 °C was 25% of that at 25 °C and increased rapidly with temperature, driven by fast adaptations of microbial community structure, metabolic network of SOC decomposition, and trophic interactions. Below 7 °C, syntrophic propionate oxidation was the rate-limiting step for CH4 production; above this threshold temperature, polysaccharide hydrolysis became rate limiting. This change was associated with a shift within the functional guild for syntrophic propionate oxidation, with Firmicutes being replaced by Bacteroidetes. Correspondingly, there was a shift from the formate- and H2-using Methanobacteriales to Methanomicrobiales and from the acetotrophic Methanosarcinaceae to Methanosaetaceae. Methanogenesis from methylamines, probably stemming from degradation of bacterial cells, became more important with increasing temperature and corresponded with an increased relative abundance of predatory protists of the phylum Cercozoa. We concluded that Arctic peat microbiota responds rapidly to increased temperatures by modulating metabolic and trophic interactions so that CH4 is always highly produced: The microbial community adapts through taxonomic shifts, and cascade effects of substrate availability cause replacement of functional guilds and functional changes within taxa.
Footnotes
- ↵1To whom correspondence may be addressed. Email: alexander.t.tveit{at}uit.no or mette.svenning{at}uit.no.
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Author contributions: A.T.T., T.U., P.F., and M.M.S. designed research; A.T.T. performed research; A.T.T. and P.F. analyzed data; and A.T.T., T.U., P.F., and M.M.S. wrote the paper.
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The authors declare no conflict of interest.
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This article is a PNAS Direct Submission.
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Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive (SRA) database, www.ncbi.nlm.nih.gov/sra (accession nos. SRX885604, SRX885607, SRX885609, SRX885611, and SRX885615–SRX885628).
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This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1420797112/-/DCSupplemental.
Freely available online through the PNAS open access option.
