Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes.

Katie Sipes,Peibo Li,Sean Schaeffer,Tullis C Onstott,Karen G Lloyd,Tatiana A Vishnivetskaya,Renxing Liang,Julia Boike,Raegan Paul,Aubrey Fine

doi:10.3389/fmicb.2021.757812

Abstract

The active layer of permafrost in Ny Ålesund, Svalbard (79°N) around the Bayelva River in the Leirhaugen glacier moraine is measured as a small net carbon sink at the brink of becoming a carbon source. In many permafrost-dominating ecosystems, microbes in the active layers have been shown to drive organic matter degradation and greenhouse gas production, creating positive feedback on climate change. However, the microbial metabolisms linking the environmental geochemical processes and the populations that perform them have not been fully characterized. In this paper, we present geochemical, enzymatic, and isotopic data paired with 10 Pseudomonas sp. cultures and metagenomic libraries of two active layer soil cores (BPF1 and BPF2) from Ny Ålesund, Svalbard, (79°N). Relative to BPF1, BPF2 had statistically higher C/N ratios (15 ± 1 for BPF1 vs. 29 ± 10 for BPF2; n = 30, p < 10–5), statistically lower organic carbon (2% ± 0.6% for BPF1 vs. 1.6% ± 0.4% for BPF2, p < 0.02), statistically lower nitrogen (0.1% ± 0.03% for BPF1 vs. 0.07% ± 0.02% for BPF2, p < 10–6). The d13C values for inorganic carbon did not correlate with those of organic carbon in BPF2, suggesting lower heterotrophic respiration. An increase in the δ13C of inorganic carbon with depth either reflects an autotrophic signal or mixing between a heterotrophic source at the surface and a lithotrophic source at depth. Potential enzyme activity of xylosidase and N-acetyl-β-D-glucosaminidase increases twofold at 15°C, relative to 25°C, indicating cold adaptation in the cultures and bulk soil. Potential enzyme activity of leucine aminopeptidase across soils and cultures was two orders of magnitude higher than other tested enzymes, implying that organisms use leucine as a nitrogen and carbon source in this nutrient-limited environment. Besides demonstrating large variability in carbon compositions of permafrost active layer soils only ∼84 m apart, results suggest that the Svalbard active layer microbes are often limited by organic carbon or nitrogen availability and have adaptations to the current environment, and metabolic flexibility to adapt to the warming climate.

Highlights

Temperatures in the Arctic are increasing faster than they are at lower latitudes (Cohen et al, 2014; Pörtner et al, 2019)
We investigated the microbial influence on two active layer geochemical profiles by combining cultured isolates with metagenomic inferences, extracellular enzyme assays, and soil geochemistry such as carbon and nitrogen content and stable isotope ratios
Carbon to nitrogen ratios (C/N) in Bayelva Permafrost Site 1 (BPF1) ranged from ∼13 to 18, and those of BPF2 increased with depth from ∼19 to 50 (Figure 2G)

Summary

Introduction

Temperatures in the Arctic are increasing faster than they are at lower latitudes (Cohen et al, 2014; Pörtner et al, 2019). Future climatic conditions are likely to increase the availability of carbon sources for microbial decomposition since temperature, water availability, and the rate of microbial carbon degradation in permafrost are related (Waldrop et al, 2010; Beermann et al, 2017; Garnello et al, 2021). Due to increases in temperature and microbial activity, this warm permafrost location could be at the brink of becoming a net source of greenhouse gasses such as CH4 and CO2. We combined soil carbon and nitrogen analysis, extracellular enzymes assays, isolate activities, and metagenomes to gain a broader view of current carbon degradation activities, and their relationship to nitrogen cycling, in Svalbard active layer soils

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