Permafrost degradation inputs shape mitigation potential of methane emissions from aquatic ecosystems in a polygonal peatland context

In polygonal peatlands, typical of continuous permafrost, numerous small aquatic ecosystems are found in ice-wedge troughs but also in larger depressions. These ponds reflect permafrost evolution and degradation, which influences their functioning. Permafrost ice is enriched in carbon and nutrients, and its degradation leads to the transfer of Dissolved Organic Carbon (DOC), nutrients (N, P) and microorganisms to ponds. These aquatic ecosystems act as CH₄ emission hotspots. An important proportion of the CH₄ produced by ponds is mitigated in the water column by methanotrophic activity. We refer to the hydrological and biological exchange between permafrost pore ice and aquatic ecosystems, which is driven by ongoing permafrost degradation, as permafrost-pond connectivity. The effects of permafrost-ponds connectivity on microbial communities and CH₄ oxidation activity remain to be assessed, to understand how permafrost degradation could influence future Greenhouse Gas (GHG) fluxes of polygonal peatland.

In this study, we combined in situ monitoring and incubation approach of small ponds of polygonal peatlands. Study sites were located near Churchill (Manitoba, Canada) and across Wapusk National Park, in the Hudson Bay lowlands, the second largest complex of permafrost peatland in the world. To investigate the diversity and functioning of aquatic ecosystems, we characterised GHG concentration and fluxes, organic carbon, nutrient concentrations and microbial communities, in and around forty waterbodies covering a large range of permafrost degradation context, from small trough ponds to larger depressions. Additionally, we tested the effect of permafrost-pond connectivity on CH₄ oxidation activity in an experimental setting by adding inorganic nutrients (N, P) or permafrost pore ice into methanotrophic incubations of pond water. Ponds selected for these experiments covered a range of different permafrost connectivity context.

We found that the degree of connectivity between permafrost ice and ponds strongly structures their microbial community composition, nutrient content and CH₄ mitigation potential. Higher connectivity to permafrost leads to higher DOC and Total Phosphorous (TP) content, whereas lower [CH₄] were measured. Nutrient transfer affected CH₄ oxidation activity in different ways in methanotrophic experiments. Synthetic NP inputs increased CH₄ oxidation activity. On the other hand, permafrost pore ice transfer led to strong decrease of CH₄ oxidation activity. Labile DOC and nutrients contained in permafrost pore ice increased heterotrophic activity and competition for O₂. Ponds with low connectivity to permafrost (influenced by the active layer) were more sensitive to nutrient inputs than the ponds highly connected with permafrost. These results suggest that methanotrophic activity could be less nutrient-limited as a result of higher nutrient input from permafrost to ponds. These results show that nutrient transfer from permafrost alters CH₄ mitigation activity and influences CH₄ emissions from aquatic ecosystems in a polygonal peatland context. This study provides new insights into understanding biogeochemical processes and estimating permafrost thaw positive feedback to climate change.