Microbial Community Changes in 26,500-Year-Old Thawing Permafrost

Abstract

Northern permafrost soils store more than half of the global soil carbon. Frozen for at least two consecutive years, but often for millennia, permafrost temperatures have increased drastically in the last decades. The resulting thermal erosion leads not only to gradual thaw, resulting in an increase of seasonally thawing soil thickness, but also to abrupt thaw events, such as sudden collapses of the soil surface. These could affect 20% of the permafrost zone and half of its organic carbon, increasing accessibility for deeper rooting vegetation and microbial decomposition into greenhouse gases. Knowledge gaps include the impact of permafrost thaw on the soil microfauna as well as key taxa to change the microbial mineralization of ancient permafrost carbon stocks during erosion. Here, we present the first sequencing study of an abrupt permafrost erosion microbiome in Northeast Greenland, where a thermal erosion gully collapsed in the summer of 2018, leading to the thawing of 26,500-year-old permafrost material. We investigated which soil parameters (pH, soil carbon content, age and moisture, organic and mineral horizons, and permafrost layers) most significantly drove changes of taxonomic diversity and the abundance of soil microorganisms in two consecutive years of intense erosion. Sequencing of the prokaryotic 16S rRNA and fungal ITS2 gene regions at finely scaled depth increments revealed decreasing alpha diversity with depth, soil age, and pH. The most significant drivers of variation were found in the soil age, horizons, and permafrost layer for prokaryotic and fungal beta diversity. Permafrost was mainly dominated by Proteobacteria and Firmicutes, with Polaromonas identified as the most abundant taxon. Thawed permafrost samples indicated increased abundance of several copiotrophic phyla, such as Bacteroidia, suggesting alterations of carbon utilization pathways within eroding permafrost.

Abrupt permafrost thaw triggers microbial bloom and grazer succession

“…This could enable dispersal into deeper soils, although we expect this to be an overall slow process as we expect an overall still low soil temperature and nutrient availability. An amplicon-based study at this site still confirmed similar emerging drivers, mainly layer and age (Scheel et al, 2022), as the only soil microbial studies performed locally before (Ganzert et al, 2014; Gittel et al, 2014b). Overall, more than half of all counts stem from taxa dominantly present in the thawed layers.…”

“…Similarly, the active Bacteroidetes order Sphingobacteriales dominated recently thawed permafrost. In our study site, this order formerly had the highest relative amplicon-based abundance with more than 50% of all counts between 70‒90 cm depth in 2020, despite very low abundances one year earlier (Scheel et al, 2022). This confirms that this taxon as a major component of the microbial community at thawed depths, which responds strongly to thaw (Burkert et al, 2019; Coolen and Orsi, 2015; Deng et al, 2015; Frank-Fahle et al, 2014) and is abundant at the upper permafrost limit (Müller et al, 2018; Tripathi et al, 2018).…”

“…Schostag and colleagues showed that the Nitrosomonadaceae relative abundance correlated with nitrogen pools in permafrost soils (Schostag et al, 2019). Here, especially the family Gallionellaceae contains nitrate-dependent ferrous iron-oxidising taxa (He et al, 2016) and was previously found in partly ancient permafrost (Alawi et al, 2007; Müller et al, 2018; Scheel et al, 2022). Notably, most genera with maximum relative abundances at this depth (70 cm), were putative ammonia oxidizers within Betaproteobacteria.…”

“…Physical soil properties from thawed triplicates per 10 cm were determined as described by Scheel and colleagues (Scheel et al, 2022). In short, weight-based relative soil moisture (H2O) and organic carbon content (SOM) were calculated by air-drying at 70 °C for 48 h and burning at 450 °C for 2 h. Radiocarbon dating was performed on sieved macrofossils.…”

“…While the role of microbial predators in temperate soils has been studied extensively (Thakur and Geisen, 2019), bacteria-protozoan interactions in thawing permafrost have not been thoroughly explored, although microbial predator presence has been documented (Malard and Pearce, 2018; Scheel et al, 2022; Schostag et al, 2019; Shatilovich et al, 2009). Previous research on thawing permafrost soil has included incubation or gradual thaw gradients, but few microbial studies were conducted on abrupt permafrost erosion sites.…”