Abstract
Permafrost is an extreme habitat yet it hosts microbial populations that remain active over millennia. Using permafrost collected from a Pleistocene chronosequence (19 to 33 ka), we hypothesized that the functional genetic potential of microbial communities in permafrost would reflect microbial strategies to metabolize permafrost soluble organic matter (OM) in situ over geologic time. We also hypothesized that changes in the metagenome across the chronosequence would correlate with shifts in carbon chemistry, permafrost age, and paleoclimate at the time of permafrost formation. We combined high-resolution characterization of water-soluble OM by Fourier-transform ion-cyclotron-resonance mass spectrometry (FT-ICR MS), quantification of organic anions in permafrost water extracts, and metagenomic sequencing to better understand the relationships between the molecular-level composition of potentially bioavailable OM, the microbial community, and permafrost age. Both age and paleoclimate had marked effects on both the molecular composition of dissolved OM and the microbial community. The relative abundance of genes associated with hydrogenotrophic methanogenesis, carbohydrate active enzyme families, nominal oxidation state of carbon (NOSC), and number of identifiable molecular formulae significantly decreased with increasing age. In contrast, genes associated with fermentation of short chain fatty acids (SCFAs), the concentration of SCFAs and ammonium all significantly increased with age. We present a conceptual model of microbial metabolism in permafrost based on fermentation of OM and the buildup of organic acids that helps to explain the unique chemistry of ancient permafrost soils. These findings imply long-term in situ microbial turnover of ancient permafrost OM and that this pooled biolabile OM could prime ancient permafrost soils for a larger and more rapid microbial response to thaw compared to younger permafrost soils.
Highlights
Permafrost underlies one-quarter of the Northern Hemisphere and contains almost half of the Earth’s soil carbon (C) (McGuire et al, 2018)
Permafrost DOC concentrations increased across the three sampled ages with %C, %N, and C:N remained remarkably consistent across the chronosequence (Table 1)
Average ammonium concentrations were higher for the oldest permafrost sample, while nitrate and nitrite concentrations were highest in the 27 ka samples, and chloride and sulfate concentrations were lowest in the 27 ka samples (Table 1)
Summary
Permafrost underlies one-quarter of the Northern Hemisphere and contains almost half of the Earth’s soil carbon (C) (McGuire et al, 2018). Warmer conditions prevalent in Beringia during the Holocene and portions of the late Pleistocene (e.g., 19–22, 30–38 ka) may have prevented accumulated OM from freezing, subjecting it to decomposition by microorganisms for centuries to millennia prior to permafrost formation (Hopkins, 1982; Hamilton et al, 1988; Jones et al, 2012; Kanevskiy et al, 2014) Microorganisms contained within this permafrost may be reflective of the type of organic material present but may have the capacity to alter its chemical characteristics over time (Heslop et al, 2019)
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