Genome-centric view of carbon processing in thawing permafrost

Ben J. Woodcroft, Caitlin M. Singleton, Joel A. Boyd, Paul N. Evans, Joanne B. Emerson, Ahmed A. F. Zayed, Robert D. Hoelzle, Timothy O. Lamberton, Carmody K. McCalley, Suzanne B. Hodgkins, Rachel M. Wilson, Samuel O. Purvine, Carrie D. Nicora, Changsheng Li, Steve Frolking, Jeffrey P. Chanton, Patrick M. Crill, Scott R. Saleska, Virginia I. Rich, Gene W. Tyson

As global temperatures rise, large amounts of carbon sequestered in permafrost are becoming available for microbial degradation. Accurate prediction of carbon gas emissions from thawing permafrost is limited by our understanding of these microbial communities. Here we use metagenomic sequencing of 214 samples from a permafrost thaw gradient to recover 1,529 metagenome-assembled genomes, including many from phyla with poor genomic representation. These genomes reflect the diversity of this complex ecosystem, with genus-level representatives for more than sixty per cent of the community. Meta-omic analysis revealed key populations involved in the degradation of organic matter, including bacteria whose genomes encode a previously undescribed fungal pathway for xylose degradation. Microbial and geochemical data highlight lineages that correlate with the production of greenhouse gases and indicate novel syntrophic relationships. Our findings link changing biogeochemistry to specific microbial lineages involved in carbon processing, and provide key information for predicting the effects of climate change on permafrost systems.