Genomic insights into redox-driven microbial processes for carbon decomposition in thawing Arctic soils and permafrost

Li, Yaoming; Xue, Yaxin; Chowdhury, Taniya Roy; Graham, David E.; Tringe, Susannah G.; Jansson, Janet K.; Taş, Neslihan

doi:10.1128/msphere.00259-24

Genomic insights into redox-driven microbial processes for carbon decomposition in thawing Arctic soils and permafrost

Journal Article · Tue Jun 11 00:00:00 EDT 2024 · mSphere

DOI:https://doi.org/10.1128/msphere.00259-24· OSTI ID:2376397

Li, Yaoming ^[1]; Xue, Yaxin ^[2]; Chowdhury, Taniya Roy ^[3]; ^[4]; ^[5]; ^[6]; ^[7]

Beijing Forest Univ. (China); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
AstraZeneca, Cambridge (United Kingdom)
Woodwell Climate Research Center, Falmouth, MA (United States)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Climate change is rapidly transforming Arctic landscapes where increasing soil temperatures speed up permafrost thaw. This exposes large carbon stocks to microbial decomposition, possibly worsening climate change by releasing more greenhouse gases. Understanding how microbes break down soil carbon, especially under the anaerobic conditions of thawing permafrost, is important to determine future changes. Here, we studied the microbial community dynamics and soil carbon decomposition potential in permafrost and active layer soils under anaerobic laboratory conditions that simulated an Arctic summer thaw. The microbial and viral compositions in the samples were analyzed based on metagenomes, metagenome-assembled genomes, and metagenomic viral contigs (mVCs). Following the thawing of permafrost, there was a notable shift in microbial community structure, with fermentative Firmicutes and Bacteroidota taking over from Actinobacteria and Proteobacteria over the 60-day incubation period. The increase in iron and sulfate-reducing microbes had a significant role in limiting methane production from thawed permafrost, underscoring the competition within microbial communities. We explored the growth strategies of microbial communities and found that slow growth was the major strategy in both the active layer and permafrost. Our findings challenge the assumption that fast-growing microbes mainly respond to environmental changes like permafrost thaw. Instead, they indicate a common strategy of slow growth among microbial communities, likely due to the thermodynamic constraints of soil substrates and electron acceptors, and the need for microbes to adjust to post-thaw conditions. The mVCs harbored a wide range of auxiliary metabolic genes that may support cell protection from ice formation in virus-infected cells.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Laboratory Directed Research and Development (LDRD) Program; National Natural Science Foundation of China (NSFC)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 2376397

Journal Information:: mSphere, Journal Name: mSphere Journal Issue: 7 Vol. 9; ISSN 2379-5042

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Metagenome-assembled genome distribution and key functionality highlight importance of aerobic metabolism in Svalbard permafrost

Journal Article · Fri Apr 17 00:00:00 EDT 2020 · FEMS Microbiology Ecology · OSTI ID:1663231

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Anaerobic carbon mineralization
Climate warming
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Permafrost
Sulfate reduction

Genomic insights into redox-driven microbial processes for carbon decomposition in thawing Arctic soils and permafrost

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