Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Microbial Networks Demonstrate Extraordinary Metabolic Versatility and the Ability to Obtain Electron Acceptors from Soil Organic Matter in Temperate Peatland Soils

Authors:

Joel E. Kostka1* (joel.kostka@biology.gatech.edu), Katherine Duchesneau1, Borja Aldeguer Riquelme1, Caitlin Petro1, Kostas Konstantinidis1, Madison Green1, Ghiwa Makke2, Malak Tfaily2, Rachel M. Wilson3, Jeffrey P. Chanton3, Christopher W. Schadt4, Paul J. Hanson4

Institutions:

1Georgia Institute of Technology–Atlanta; 2University of Arizona–Tucson; 3Florida State University–Tallahassee; 4Oak Ridge National Laboratory

Goals

The goal of this project is to elucidate the fundamental principles driving physiology and metabolic exchange within microbial interaction networks that regulate the rate-limiting steps in soil organic matter (SOM) degradation, specifically the oxidation of phenolic compounds derived from lignocellulose and lignin-like polymers in carbon-rich peatlands and their role in the preservation of organic matter under anaerobic, water-saturated conditions. The project combines multiomics with advanced analytical chemistry to test the “enzyme latch” hypothesis and its response to climate change drivers. Field and laboratory investigations will be integrated to construct and calibrate a predictive framework that links specific microbial processes and interactions to the mechanisms driving the rate-limiting steps of enzymatic SOM decomposition (phenolic compound oxidation and hydrolysis), SOM persistence, and greenhouse gas production in peatland soils. To investigate the response of microbial communities to climate change drivers, researchers leverage DOE’s Spruce and Peatland Responses under Changing Environments (SPRUCE) experiment where air and peat warming are combined in a whole ecosystem warming treatment.

Abstract

Peatlands represent climate critical regions that cover only 3% of the Earth’s land surface but store approximately 1/3 of all soil carbon (C). The future role of peatlands in C sequestration remains uncertain and depends on the impact of global change-related perturbations on their C balance. In this project, researchers defined the microbial networks that regulate belowground C turnover by combining a genomic-centric metagenomics approach with biogeochemistry and metabolomics. The team analyzed 131 metagenomes (totaling 2.4 Tbp of sequences) obtained from soil samples collected to 2 meters depth in the peat column between 2015 and 2018, reconstructing 697 metagenome-assembled genomes (MAGs). Surprisingly, researchers found that only 2% of the MAGs retrieved from the SPRUCE site were shared with those identified in well-studied European peatlands where soils experience similar environmental conditions. Microbial community composition and functional potential are strongly depth-stratified and closely parallel changes in activity, redox, and organic matter quality. Overall, the metabolic pathways identified within the MAGs reveal a high-metabolic potential for sulfate/sulfite reduction, denitrification, methanogenesis, and homoacetogenesis, implicating, which are important terminal electron accepting processes. The dominant methanogens detected (Methanoflorens) demonstrate the potential to carry out acetoclastic as well as hydrogenotrophic methanogenesis, which has been only described previously for the genus Methanosarcina. In addition, the team uncovered a large diversity of sulfate/sulfite reducers and acetogens that were not previously associated with peatlands. The results indicate that C degradation is electron acceptor-limited and mediated by a much broader repertoire of anaerobic respiration processes than previously thought, likely supplied by electron acceptors derived from the soil organic matter itself. Despite the dramatic increase in gaseous emissions (e.g., carbon dioxide, methane) with warming over the same period, microbial diversity and composition remained stable, indicating slow growth and a resistant soil ecosystem. However, the genomic potential for methylotrophic methanogenesis was stimulated while homoacetogenesis was hampered by warming.

Reseachers took advantage of a generational drought that occurred in 2021 at the SPRUCE site to investigate the combined impacts of warming and drought on the belowground C cycle. The team hypothesized that the warmed, dried peatland will be released from the “enzyme latch,” thereby accelerating soil organic matter decomposition by enhancing the oxidation of phenolic compounds. During and postdrought, phenolic degradation and C-activated gene expression as well as enzyme activity increased, likely driven by heightened fungal activity.

Conversely, climate change-induced water-table drawdown reduced the activity of versatile polyphenol-degraders as well as the expression of anaerobic phenolic compound transforming genes. Temperature influenced the microbial community’s recovery postdrought, with warmer treatments exhibiting gene-expression patterns more divergent from the predrought profile compared to ambient conditions. This research indicates that phenolic compound degradation is more complex than the “enzyme latch” suggests, emphasizing the need for a deeper understanding of microbial processes to accurately predict the impact of climate change on peatland C storage.

To determine whether warming-induced shifts in plant species composition may act to bolster the “enzyme latch” through the accumulation of plant-derived phenolic compounds that inhibit microbial SOM decomposition, the team conducted a seasonal study of soluble phenolic compound concentrations across the SPRUCE temperature treatments. Phenolic compounds are highly sensitive to temperature and exhibit the greatest concentrations (by a factor of four) in the warmest treatments where shrubs, coincidentally, have significantly increased in biomass relative to other types of vegetation. Phenolic compounds, normalized to total dissolved organic matter (DOM) concentration, show a 50% increase across seasons in all plots. This data indicate that both phenolic compounds and DOM increase with growing season and temperature, but that phenolic compounds are either more recalcitrant over the annual cycle or they are produced and retained at a higher rate. In addition, researchers performed a comparison of peatland sites that vary in plant species composition, temperature, and pH (3.5 to 6.5) across a latitudinal gradient, and the team observed a significant negative correlation between soil pH and soluble phenolics with low pH sites showing up to 5-fold higher phenolic concentrations. Researchers are currently quantifying decomposition rates in soils from all peatlands sampled to explore the controls of C turnover across peatland types.

Funding Information

This research was supported by the DOE Office of Science, BER program, grant no. DE-SC0023297.