One quarter of the earth’s terrestrial surface is underlain by permafrost, or perennially frozen soils. Permafrost soils contain approximately 25-50% of the total global soil C pool, nearly double the atmospheric C reservoir. The C is largely protected from microbial decomposition by frozen conditions, but climate change is threating to induce large-scale permafrost thaw exposing it to degradation. The resulting production of globally significant quantities of greenhouse gasses (GHGs)—including CO2, CH4, and N2O—is expected to result in a positive feedback loop thus amplifying the effects of global warming. Chemically, much of the permafrost contains a high proportion of easily decomposed material, but this does not mean the permafrost is uniform and that similar microbial communities and similar thaw responses should be expected. Permafrost only defines the thermal state of soil and thus the chemistry and age can differ among locations due to inputs, sequestration processes, and decomposition processes. In this study, we compared how permafrost age, history, and chemistry drives the ability of microbial communities to degrade carbon. We combined deep metagenomic sequencing of microbial communities and fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) of carbon composition across a Pleistocene permafrost chronosequence from 19,000 to 33,000 years before present (kyr).
We found that microbial communities adapt to life in permafrost through geologic time as evidenced by an increasing abundance of genes involved in the survival under frozen static conditions. However, the ability to degrade carbon was not influenced by age. Instead, carbon processing genes were correlated with carbon composition, vegetation present at the time the permafrost formed (as determined by the paleovegetation reconstruction from metagenomic sequence), and paleoclimate. Here, we describe how carbon processing capabilities are related to carbon chemistry and the paleoenvironment and how the ability to degrade carbon is partitioned among different community members. The ultimate fate of carbon from permafrost depends on the complex relationship between permafrost physiochemistry and microbial communities. Therefore, understanding how the two interact will be important for predicting greenhouse gas emissions from the thawing permafrost.