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Microbes Metabolize Polyphenols in Anoxic Wetland Soil

These results challenge presumed metabolic roles of soil microbes in long-held views of soil nutrient cycling. 

illustration of polyphenol metabolism with background illustrating soil
Research performed under the Facilities Integrating Collaborations for User Science, known as "FICUS," initiative results in new thinking about an old theory. Image by Stephanie King  |  Pacific Northwest National Laboratory

The Science  

According to a long-held theory, plant secondary metabolites called polyphenols resist being broken down by microbes under low oxygen conditions in peat soils. A multi-institutional team of scientists tested this assumption in a soil system. They added a chemically-defined polyphenol to anoxic soil reactors. Then the scientists measured the metabolic activity of the soil microbes using large-scale measurements of metabolites and microbial proteins. Some soil microbes did degrade polyphenols. 

The Impact 

According to a theory called the enzyme latch model, polyphenols accumulate in anoxic soils. This polyphenol accumulation is thought to diminish microbial activity and reduce nutrient cycling. However, this study challenges this theory and represents a critical first step in describing microbial polyphenol metabolism in an anoxic soil and expanding the metabolic roles of soil microbes in long-held models of soil nutrient cycling.  

Summary 

The scientists added surface soil from a well-studied wetland to an anoxic soil reactor. Then they amended this microenvironment with a structurally characterized condensed tannin. Samples of the microenvironment were collected at regular intervals, and members of the microbial community were identified by metagenomic sequencing and analysis. The scientists also measured metabolites and proteins from the model soil microbiome at various times for 20 days using metaproteomics, NMR metabolomics, and high-resolution mass spectrometry.  

The multi-institutional team measured metabolites in soil reactors containing microbes that were fed the condensed tannin. Then, the team compared those metabolites with those measured from  sterilized soil reactors containing the same molecule. These results indicated microbes break down this polyphenol, causing the accumulation of small phenolic molecules. Using genome-resolved metaproteomics data, the team identified specific members of the microbial community that were most active in soil amended with condensed tannin. These measurements indicate that the soil microbiome function is maintained, and possibly enhanced, with the addition of polyphenol. 

This research was performed under the Facilities Integrating Collaborations for User Science (FICUS)  initiative and used resources at the Department of Energy (DOE) Joint Genome Institute (JGI) and Environmental Molecular Sciences Laboratory (EMSL), which are DOE Office of Science user facilities.  

Contact 

Kelly Wrighton 
Colorado State University 
Kelly.Wrighton@ColoState.edu  

Funding 

National Science Foundation (Early Career Award); DOE Office of Science, Biological and Environmental Research program (Early Career Award and Genomic Sciences program); DOE Office of Biological and Environmental Research FICUS program for resources at JGI and EMSL, which are DOE Office of Science user facilities; and National Energy Research Scientific Computing Center. 

Publication 

B.B. McGivern, et al. “Decrypting bacterial polyphenol metabolism in an anoxic wetland soil.” Nature Communications 12, 2466 (2021). [DOI: 10.1038/s41467-021-22765-1]