Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms

Abstract

A substantial part of the Earths' soil organic carbon (SOC) is stored in Arctic permafrost peatlands, which represent large potential sources for increased emissions of the greenhouse gases CH(4) and CO(2) in a warming climate. The microbial communities and their genetic repertoire involved in the breakdown and mineralisation of SOC in these soils are, however, poorly understood. In this study, we applied a combined metagenomic and metatranscriptomic approach on two Arctic peat soils to investigate the identity and the gene pool of the microbiota driving the SOC degradation in the seasonally thawed active layers. A large and diverse set of genes encoding plant polymer-degrading enzymes was found, comparable to microbiotas from temperate and subtropical soils. This indicates that the metabolic potential for SOC degradation in Arctic peat is not different from that of other climatic zones. The majority of these genes were assigned to three bacterial phyla, Actinobacteria, Verrucomicrobia and Bacteroidetes. Anaerobic metabolic pathways and the fraction of methanogenic archaea increased with peat depth, evident for a gradual transition from aerobic to anaerobic lifestyles. A population of CH(4)-oxidising bacteria closely related to Methylobacter tundripaludum was the dominating active group of methanotrophs. Based on the in-depth characterisation of the microbes and their genes, we conclude that these Arctic peat soils will turn into CO(2) sources owing to increased active layer depth and prolonged growing season. However, the extent of future CH(4) emissions will critically depend on the response of the methanotrophic bacteria.

Figure 1

Three-domain community profile of the microbiota in Svalbard peatlands. The figures are based on the ribo-tags fraction of the metatranscriptome. The size of the boxes is proportional to the fraction of ribo-tags of the respective taxa. (a) Top layer of Solvatn peat generated from two biological replicate data sets (S1a and S2a). (b) Lower layer of Solvatn generated from one data set (S2b). (c) Top layer of Knudsenheia peat generated from two biological replicate data sets (K1a and K2a). Asco, Ascomycota; Basidio, Basidiomycota; Meth.bac., Methanobacteriales; Meth.mic., Methanomicrobiales; Meth.sarc., Methanosarcinales.

Figure 2

Taxonomic assignment of metatranscriptomic and metagenomic sequences. The community structure is displayed at phylum level resolution with Proteobacteria split into classes. Sequences assigned to Proteobacteria refer to sequences that could not be assigned to class level resolution. S2 and K1 indicates where the samples were collected, in Solvatn and Knudsenheia respectively, while a, b and c indicates the depth of the sample from top and down (Supplementary Figure S3). (a) Taxonomic assignment of ribo-tags, mRNA and metagenomic DNA (gDNA) to the domain bacteria. (b) Taxonomic assignment of the metagenomic sequences encoding polysaccharide-degrading enzymes (cellulases, endohemicellulases and debranching enzymes). All sequences assigned to these categories were pooled together and taxonomically binned using MEGAN (see Materials and methods for details).

Figure 3

M. tundripaludum in Svalbard peat soils. The phylogenetic tree shows assembled SSU rRNA contigs of type I methanotrophs. Most of the nearly full-length ribo-contigs (14 out of 16) are >97% identical to M. tundripaludum. Ribo-contig description includes the following: contig id, site (Knudsenheia-green, Solvatn-red), contig length and the number of single ribo-tags that went into the assembly. The reference sequence description (black) includes sequence length and accession number. The length of the bar indicates 0.10 changes per nucleotide. The tree was constructed using the ARB software (See Materials and methods for details). The insert shows the nitrate reductase (open reading frames (ORFs) 3936–3940) and nitrite reductase operons (ORFs 3936–3940) identified in the genome of M. tundripaludum.

Figure 4

Schematic overview of the main degradation pathways of plant polymers in the high-Arctic peatlands of Svalbard. The pathways are divided into three categories; aerobic (beige), anaerobic (light brown) and processes occurring under both conditions (dark brown). Key microbial taxa for the different degradation steps are presented (orange boxes). The figure is adapted from Figure 1 in (Conrad, 1999).