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

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 o...

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Main Authors: Katie Sipes, Raegan Paul, Aubrey Fine, Peibo Li, Renxing Liang, Julia Boike, Tullis C. Onstott, Tatiana A. Vishnivetskaya, Sean Schaeffer, Karen G. Lloyd
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-02-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.757812/full
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author Katie Sipes
Raegan Paul
Aubrey Fine
Peibo Li
Renxing Liang
Julia Boike
Julia Boike
Tullis C. Onstott
Tatiana A. Vishnivetskaya
Sean Schaeffer
Karen G. Lloyd
author_facet Katie Sipes
Raegan Paul
Aubrey Fine
Peibo Li
Renxing Liang
Julia Boike
Julia Boike
Tullis C. Onstott
Tatiana A. Vishnivetskaya
Sean Schaeffer
Karen G. Lloyd
author_sort Katie Sipes
collection DOAJ
description 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.
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spelling doaj.art-187df9cdd6a949b2bda66e223c9b2d3b2022-12-22T04:11:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-02-011210.3389/fmicb.2021.757812757812Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading EnzymesKatie Sipes0Raegan Paul1Aubrey Fine2Peibo Li3Renxing Liang4Julia Boike5Julia Boike6Tullis C. Onstott7Tatiana A. Vishnivetskaya8Sean Schaeffer9Karen G. Lloyd10Microbiology Department, University of Tennessee, Knoxville, Knoxville, TN, United StatesMicrobiology Department, University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Biosystems Engineering and Soil Science, University of Tennessee, Knoxville, Knoxville, TN, United StatesMicrobiology Department, University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Geosciences, Princeton University, Princeton, NJ, United StatesAlfred Wegener Institute, Potsdam, GermanyGeography Department, Humboldt-Universität zu Berlin, Berlin, GermanyDepartment of Geosciences, Princeton University, Princeton, NJ, United StatesCenter for Environmental Biotechnology, University of Tennessee, Knoxville, Knoxville, TN, United StatesDepartment of Biosystems Engineering and Soil Science, University of Tennessee, Knoxville, Knoxville, TN, United StatesMicrobiology Department, University of Tennessee, Knoxville, Knoxville, TN, United StatesThe 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.757812/fullSvalbardpermafrostactive layercarbonnitrogenmetagenome
spellingShingle Katie Sipes
Raegan Paul
Aubrey Fine
Peibo Li
Renxing Liang
Julia Boike
Julia Boike
Tullis C. Onstott
Tatiana A. Vishnivetskaya
Sean Schaeffer
Karen G. Lloyd
Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes
Frontiers in Microbiology
Svalbard
permafrost
active layer
carbon
nitrogen
metagenome
title Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes
title_full Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes
title_fullStr Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes
title_full_unstemmed Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes
title_short Permafrost Active Layer Microbes From Ny Ålesund, Svalbard (79°N) Show Autotrophic and Heterotrophic Metabolisms With Diverse Carbon-Degrading Enzymes
title_sort permafrost active layer microbes from ny alesund svalbard 79°n show autotrophic and heterotrophic metabolisms with diverse carbon degrading enzymes
topic Svalbard
permafrost
active layer
carbon
nitrogen
metagenome
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.757812/full
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