Hot moment of N2O emissions in seasonally frozen peatlands

Abstract

Since the start of the Anthropocene, northern seasonally frozen peatlands have been warming at a rate of 0.6 °C per decade, twice that of the Earth's average rate, thereby triggering increased nitrogen mineralization with subsequent potentially large losses of nitrous oxide (N₂O) to the atmosphere. Here we provide evidence that seasonally frozen peatlands are important N₂O emission sources in the Northern Hemisphere and the thawing periods are the hot moment of annual N₂O emissions. The flux during the hot moment of thawing in spring was 1.20 ± 0.82 mg N₂O m^-2 d^-1, significantly higher than that during the other periods (freezing, -0.12 ± 0.02 mg N₂O m^-2 d^-1; frozen, 0.04 ± 0.04 mg N₂O m^-2 d^-1; thawed, 0.09 ± 0.01 mg N₂O m^-2 d^-1) or observed for other ecosystems at the same latitude in previous studies. The observed emission flux is even higher than those of tropical forests, the World's largest natural terrestrial N₂O source. Furthermore, based on soil incubation with ¹⁵N and ¹⁸O isotope tracing and differential inhibitors, heterotrophic bacterial and fungal denitrification was revealed as the main source of N₂O in peatland profiles (0-200 cm). Metagenomic, metatranscriptomic, and qPCR assays further revealed that seasonally frozen peatlands have high N₂O emission potential, but thawing significantly stimulates expression of genes encoding N₂O-producing protein complexes (hydroxylamine dehydrogenase (hao) and nitric oxide reductase (nor)), resulting in high N₂O emissions during spring. This hot moment converts seasonally frozen peatlands into an important N₂O emission source when it is otherwise a sink. Extrapolation of our data to all northern peatland areas reveals that the hot moment emissions could amount to approximately 0.17 Tg of N₂O yr^-1. However, these N₂O emissions are still not routinely included in Earth system models and global IPCC assessments.

Fig. 1. Hot moment of N₂O emissions in seasonally frozen peatland.

A Photos showing the sampling site in different periods and the 200 cm-soil profile of sampling site E. “FL.” and “WT.” indicate the frozen layer and water table, respectively. B Site-scale in-situ N₂O fluxes in the seasonally frozen peatland. The blue curve is the Gaussian fit of the N₂O fluxes. Gas samples were collected in March, May, July, September, and November 2019, as well as in January 2020. C Regional scale in-situ N₂O fluxes in April, May, and June in 2020 at sites along the Gudong River. D Box plots showing the N₂O fluxes of the regional-scale sites (above), and box plots showing N₂O fluxes from this study compared with other ecosystems at the same latitude (below) (the horizontal line indicates the median, while the box shows the 25^th and 75^th percentiles). The abbreviations “wetl.,” “peatl.,” and “upl.” indicate wetland, peatland, and upland, respectively [13, 96]. Two and three asterisks indicate p < 0.01 and p < 0.001, respectively.

Fig. 2. Rates and contributions of bacterial, fungal denitrification and nitrification to N₂O production in the seasonally frozen peatland.

A Potential rates of bacterial denitrification, fungal denitrification, and nitrification pathways to the total N₂O production over a whole year in the seasonally frozen peatland, as determined using inhibitor methods. For each sampling month, the pie chart represents the average proportions of the three processes for the 2-m soil core. “BD.,” “FD.,” “MN.,” “AP.,” “FL.,” and “WT.” indicate bacterial denitrification, fungal denitrification, microbial nitrification, abiotic processes, frozen layer, and water table, respectively. The stacked area plot shows the contributions of bacterial denitrification, fungal denitrification, nitrification, and abiotic processes to N₂O production. B Contributions of nitrifier nitrification (NN), nitrifier denitrification (ND), nitrification-coupled denitrification (NCD), and heterotrophic denitrification (HD) pathways in the surface peat to N₂O production, as determined using isotopic ¹⁵N⁻¹⁸O techniques.

Fig. 3. N₂O production- and reduction-related functional gene transcripts identified in seasonally frozen peatland.

A Histogram showing the transcripts of N₂O production genes in the seasonally frozen peatland across a whole year as derived from metatranscriptomic data. “NA” indicates RNA concentrations that were below the detection limit for metatranscriptomic sequencing. TPM means transcripts per million. B The box plots show the relative abundance of N₂O production- and reduction-related functional gene based on RNA data (the horizontal line indicates the median, while the box shows the 25^th and 75^th percentiles). “Tot. pro.” and “Tot. red.” indicate total production and total reduction, respectively. One, two, and three asterisks indicate p < 0.05, p < 0.01, and p < 0.001, respectively. The months of peak abundance were highlighted for N₂O production (light purple) and reduction (light yellow) genes. C Co-occurrence network analysis showing the interaction among active N₂O production- and reduction-related microorganisms during different periods of the seasonally frozen peatland. Node colors indicate the types of genes. Edges are colored according to the interactions among different genes. The abbreviations “pro.” and “red.” indicate production and reduction, respectively.

Fig. 4. Metabolic reconstruction and features of N₂O production- and reduction-related microorganisms identified in seasonally frozen peatland.

Metabolic features across selected metagenome assembled genome (MAG) phylogenetic clusters. MAGs with the nirK gene were selected for phylogeny construction. Having any one or more functional genes in a MAG that performs the same process is indicated by “Present.” Bootstrap support values for 1000 replicates are indicated at each node.