Linking microbial Sphagnum degradation and acetate mineralization in acidic peat bogs: from global insights to a genome-centric case study

Abstract

Ombrotrophic bogs accumulate large stores of soil carbon that eventually decompose to carbon dioxide and methane. Carbon accumulates because Sphagnum mosses slow microbial carbon decomposition processes, leading to the production of labile intermediate compounds. Acetate is a major product of Sphagnum degradation, yet rates of hydrogenotrophic methanogenesis far exceed rates of aceticlastic methanogenesis, suggesting that alternative acetate mineralization processes exist. Two possible explanations are aerobic respiration and anaerobic respiration via humic acids as electron acceptors. While these processes have been widely observed, microbial community interactions linking Sphagnum degradation and acetate mineralization remain cryptic. In this work, we use ordination and network analysis of functional genes from 110 globally distributed peatland metagenomes to identify conserved metabolic pathways in Sphagnum bogs. We then use metagenome-assembled genomes (MAGs) from McLean Bog, a Sphagnum bog in New York State, as a local case study to reconstruct pathways of Sphagnum degradation and acetate mineralization. We describe metabolically flexible Acidobacteriota MAGs that contain all genes to completely degrade Sphagnum cell wall sugars under both aerobic and anaerobic conditions. Finally, we propose a hypothetical model of acetate oxidation driven by changes in peat redox potential that explain how bogs may circumvent aceticlastic methanogenesis through aerobic and humics-driven respiration.

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Fig. 1: PCA of 110 peatland metagenome samples from 12 sites based on functional gene abundance for enzymes annotated by enzyme classification (EC) value using KEGG pathway categories.
Fig. 2: Tree: taxonomic composition and relative abundance of MAGs from MB.
Fig. 3: Metabolic reconstruction of central metabolic reactions utilizing products of Sphagnum-degrading glycoside hydrolase reactions in 69 Sphagnum-degrading MAGs.

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Acknowledgements

The authors would like to thank Tamar Barkay, Hinsby Cadillo-Quiroz, and Janet Jansson for their permission to include their unpublished metagenomes in this study. This work was supported by a microbial/metagenome project (CSP 503730) through the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, which is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02–05CH11231.

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St. James, A.R., Yavitt, J.B., Zinder, S.H. et al. Linking microbial Sphagnum degradation and acetate mineralization in acidic peat bogs: from global insights to a genome-centric case study. ISME J (2020). https://doi.org/10.1038/s41396-020-00782-0

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