Metabolic and trophic interactions modulate methane production by Arctic peat microbiota in response to warming.
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.
Department of Arctic and Marine Biology, University of Tromsø The Arctic University of Norway, 9037 Tromsø, Norway; alexander.t.tveit@uit.no mette.svenning@uit.no.
Alexander Tøsdal
AT
Tveit
Department of Ecogenomics and Systems Biology, University of Vienna, 1090 Vienna, Austria; Austrian Polar Research Institute, 1090, Vienna, Austria; and.
Tim
T
Urich
Department of Biochemistry, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany.
Peter
P
Frenzel
Department of Arctic and Marine Biology, University of Tromsø The Arctic University of Norway, 9037 Tromsø, Norway; alexander.t.tveit@uit.no mette.svenning@uit.no.
Mette Marianne
MM
Svenning
D001105:Archaea / Q000235:genetics / Q000378:metabolism*; D001110:Arctic Regions; D002244:Carbon / Q000737:chemistry; D002245:Carbon Dioxide / Q000737:chemistry; D002849:Chromatography, Gas; D002851:Chromatography, High Pressure Liquid; D017753:Ecosystem; D004777:Environment; D005285:Fermentation; D020869:Gene Expression Profiling; D057232:Global Warming; D006859:Hydrogen / Q000737:chemistry; D006868:Hydrolysis; D016014:Linear Models; D008697:Methane / Q000096:biosynthesis*; D064307:Microbiota; D011134:Polysaccharides / Q000737:chemistry; D012335:RNA, Ribosomal / Q000378:metabolism; D012987:Soil / Q000737:chemistry; D012988:Soil Microbiology; D044003:Sphagnopsida; D013696:Temperature
D011134:Polysaccharides; D012335:RNA, Ribosomal; D012987:Soil; D002245:Carbon Dioxide; D002244:Carbon; D006859:Hydrogen; D008697:Methane
Arctic peat; SOC mineralization; methane; microorganisms; temperature