Ontogenic succession of thermokarst thaw ponds is linked to dissolved organic matter quality and microbial degradation potential

Abstract

Warming climate is thawing the permafrost in arctic and subarctic regions, leading to formation of thermokarst ponds. During the formation and geomorphological succession of these ponds, carbon that has been trapped in frozen soils for thousands of years is hydrologically mobilized and returned to the active carbon cycle. We sampled 12 thermokarst ponds representing three different stages of pond succession to study the potential of microbial communities to metabolize the organic carbon in the water. We investigated the quality of the dissolved organic carbon (DOC) in the water column based on the spectrophotometric and fluorometric properties of the chromophoric dissolved organic matter combined with parallel factor analysis and the potential of the microbial community for degrading these carbon compounds based on genetic markers related to carbon degradation. Our analysis showed a clear difference in the DOC quality across the different developmental stages. In the younger ponds, organic matter quality suggested that it was originating from the degrading permafrost and in the metagenomes collected from these ponds, the normalized abundance of genes related to degradation of carbon compounds was higher. There was also a shift in the degradation potential in the water column of the ponds, with higher potential for organic matter degradation in deeper, anoxic layers. In conclusion, our results show that the DOC quality and the genetic potential of the microbial community for carbon cycling change across the pond ontogeny, suggesting a capacity of the microbial communities to adapt to changing environmental conditions. Permafrost soils contain one of the major carbon storages on Earth, with an estimated 950-1672 Gt of carbon (Zimov et al.

The biogeochemical variability of Arctic thermokarst ponds is reflected by stochastic and niche‐driven microbial community assembly processes

“…Since the ponds were situated within the beds of two ancient thaw lakes of different drainage age, it is conceivable that the composition of the active layer and permafrost in carbon and ice might differ as well. The geomorphological origin and maturation of thermokarst ponds also influence the amount of C discharged into ponds (Pokrovsky et al ., 2011; Peura et al ., 2020). The banks of trough ponds appeared to be less stable than of the polygonal ones, as indicated by the presence of flooded Betula nana .…”

Dissolved organic matter biodegradation along a hydrological continuum in permafrost peatlands

“…For these reasons, coupled aquatic-soil studies of organic matter (OM) in continuous-discontinuous permafrost regions are needed (Vonk et al, 2019). The importance of surface waters from frozen peatlands in DOC processing and CO2 emissions motivated numerous studies of aquatic DOM (Hulatt et al, 2014;Manasypov et al, 2015;Mann et al, 2015Mann et al, , 2012Peura et al, 2020;Pokrovsky et al, 2016;Shirokova et al, 2019). The latter study in NE European tundra peatlands demonstrated weak biodegradation of DOM along a hydrological continuum from peatland subsidence to a large river (Pechora) and suggested that CO2 emission from surface waters could be explained either by sediment respiration or by fast processing of fresh suprapermafrost flow delivered from peat pore water and thawing soil ice.…”

Fungal community composition along a gradient of permafrost thaw

“…The vast amount of organic matter released from degrading permafrost ends up in these ponds 4 , where it can sink and be stored in the sediment, or be recycled in the microbial loop, generating greenhouse gases (GHG) as end products 5,6 . Most of the research on the microbial activity in thermokarst ponds concentrates on prokaryotes [7][8][9][10] , and despite the central role of fungi as decomposers of the organic matter in terrestrial ecosystems [11][12][13] , very little is known about the fungal communities in thermokarst ponds. To our knowledge only one study has specifically targeted the fungi in thermokarst ponds, highlighting that a major part of aquatic fungal community growing inside sporadic permafrost region belongs to unknown phyla 14 .…”