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 CH4 and CO2 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 CH4-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 CO2 sources owing to increased active layer depth and prolonged growing season. However, the extent of future CH4 emissions will critically depend on the response of the methanotrophic bacteria.
SignificanceMicroorganisms 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.
The high numbers and diversity of protists in soil systems have long been presumed, but their true diversity and community composition have remained largely concealed. Traditional cultivation-based methods miss a majority of taxa, whereas molecular barcoding approaches employing PCR introduce significant biases in reported community composition of soil protists. Here, we applied a metatranscriptomic approach to assess the protist community in 12 mineral and organic soil samples from different vegetation types and climatic zones using small subunit ribosomal RNA transcripts as marker. We detected a broad diversity of soil protists spanning across all known eukaryotic supergroups and revealed a strikingly different community composition than shown before. Protist communities differed strongly between sites, with Rhizaria and Amoebozoa dominating in forest and grassland soils, while Alveolata were most abundant in peat soils. The Amoebozoa were comprised of Tubulinea, followed with decreasing abundance by Discosea, Variosea and Mycetozoa. Transcripts of Oomycetes, Apicomplexa and Ichthyosporea suggest soil as reservoir of parasitic protist taxa. Further, Foraminifera and Choanoflagellida were ubiquitously detected, showing that these typically marine and freshwater protists are autochthonous members of the soil microbiota. To the best of our knowledge, this metatranscriptomic study provides the most comprehensive picture of active protist communities in soils to date, which is essential to target the ecological roles of protists in the complex soil system.
The functioning of Arctic soil ecosystems is crucially important for global climate, and basic knowledge regarding their biogeochemical processes is lacking. Nitrogen (N) is the major limiting nutrient in these environments, and its availability is strongly dependent on nitrification. However, microbial communities driving this process remain largely uncharacterized in Arctic soils, namely those catalyzing the rate-limiting step of ammonia (NH 3 ) oxidation. Eleven Arctic soils were analyzed through a polyphasic approach, integrating determination of gross nitrification rates, qualitative and quantitative marker gene analyses of ammonia-oxidizing archaea (AOA) and bacteria (AOB) and enrichment of AOA in laboratory cultures. AOA were the only NH 3 oxidizers detected in five out of 11 soils and outnumbered AOB in four of the remaining six soils. The AOA identified showed great phylogenetic diversity and a multifactorial association with the soil properties, reflecting an overall distribution associated with tundra type and with several physico-chemical parameters combined. Remarkably, the different gross nitrification rates between soils were associated with five distinct AOA clades, representing the great majority of known AOA diversity in soils, which suggests differences in their nitrifying potential. This was supported by selective enrichment of two of these clades in cultures with different NH 3 oxidation rates. In addition, the enrichments provided the first direct evidence for NH 3 oxidation by an AOA from an uncharacterized Thaumarchaeota-AOA lineage. Our results indicate that AOA are functionally heterogeneous and that the selection of distinct AOA populations by the environment can be a determinant for nitrification activity and N availability in soils.
The global atmospheric level of methane (CH4), the second most important greenhouse gas, is currently increasing by ∼10 million tons per year. Microbial oxidation in unsaturated soils is the only known biological process that removes CH4from the atmosphere, but so far, bacteria that can grow on atmospheric CH4have eluded all cultivation efforts. In this study, we have isolated a pure culture of a bacterium, strain MG08 that grows on air at atmospheric concentrations of CH4[1.86 parts per million volume (p.p.m.v.)]. This organism, namedMethylocapsa gorgona, is globally distributed in soils and closely related to uncultured members of the upland soil cluster α. CH4oxidation experiments and13C-single cell isotope analyses demonstrated that it oxidizes atmospheric CH4aerobically and assimilates carbon from both CH4and CO2. Its estimated specific affinity for CH4(a0s) is the highest for any cultivated methanotroph. However, growth on ambient air was also confirmed forMethylocapsa acidiphilaandMethylocapsa aurea, close relatives with a lower specific affinity for CH4, suggesting that the ability to utilize atmospheric CH4for growth is more widespread than previously believed. The closed genome ofM. gorgonaMG08 encodes a single particulate methane monooxygenase, the serine cycle for assimilation of carbon from CH4and CO2, and CO2fixation via the recently postulated reductive glycine pathway. It also fixes dinitrogen and expresses the genes for a high-affinity hydrogenase and carbon monoxide dehydrogenase, suggesting that atmospheric CH4oxidizers harvest additional energy from oxidation of the atmospheric trace gases carbon monoxide (0.2 p.p.m.v.) and hydrogen (0.5 p.p.m.v.).
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