Journal Article

Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming

Svenning, Mette Marianne, Tveit, Alexander Tøsdal, Urich, Tim, Frenzel, Peter

2015

Overview

Arctic permafrost soils store large amounts of soil organic carbon (SOC) that could be released into the atmosphere as methane (CH ₄) in a future warmer climate. How warming affects the complex microbial network decomposing SOC is not understood. We studied CH ₄ 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 CH ₄ 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 CH ₄ 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 H ₂-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 CH ₄ 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. 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.

• Publisher: National Academy of Sciences
• Subject: Archaea - genetics / Archaea - metabolism / Arctic region / Arctic Regions / Atmosphere / Biological Sciences / carbon / Carbon - chemistry / Carbon Dioxide - chemistry / Chromatography, Gas / Chromatography, High Pressure Liquid / Community structure / Ecosystem / Environment / Fermentation / Firmicutes / Gene Expression Profiling / Genomics / Global Warming / greenhouse gas emissions / greenhouse gases / Hydrogen - chemistry / Hydrolysis / Linear Models / Metabolism / Methane / Methane - biosynthesis / methane production / Methanogenesis / Methanomicrobiales / Methanosaetaceae / Methanosarcinaceae / Microbiology / Microbiota / microorganisms / Organic carbon / Oxidation / Peat / Peat soils / Permafrost / PNAS Plus / Polysaccharides - chemistry / Relative abundance / RNA, Ribosomal - metabolism / Soil - chemistry / Soil Microbiology / Sphagnopsida / Taxonomy / Temperature / Temperature gradients / Trophic relationships