Microbial Communities Influence Soil Dissolved Organic Carbon Concentration by Altering Metabolite Composition

Tayte P Campbell; Danielle E M Ulrich; Jason Toyoda; Jaron Thompson; Brian Munsky; Michaeline B N Albright; Vanessa L Bailey; Malak M Tfaily; John Dunbar

doi:10.3389/fmicb.2021.799014

Microbial Communities Influence Soil Dissolved Organic Carbon Concentration by Altering Metabolite Composition

Front Microbiol. 2022 Jan 20:12:799014. doi: 10.3389/fmicb.2021.799014. eCollection 2021.

Authors

Tayte P Campbell¹, Danielle E M Ulrich², Jason Toyoda³, Jaron Thompson⁴, Brian Munsky⁴, Michaeline B N Albright², Vanessa L Bailey¹, Malak M Tfaily⁵, John Dunbar²

Affiliations

¹ Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA, United States.
² Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM, United States.
³ Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, United States.
⁴ Department of Chemical and Biological Engineering, Colorado State University, Fort Collins, CO, United States.
⁵ Department of Environmental Science, The University of Arizona, Tucson, AZ, United States.

Abstract

Rapid microbial growth in the early phase of plant litter decomposition is viewed as an important component of soil organic matter (SOM) formation. However, the microbial taxa and chemical substrates that correlate with carbon storage are not well resolved. The complexity of microbial communities and diverse substrate chemistries that occur in natural soils make it difficult to identify links between community membership and decomposition processes in the soil environment. To identify potential relationships between microbes, soil organic matter, and their impact on carbon storage, we used sand microcosms to control for external environmental factors such as changes in temperature and moisture as well as the variability in available carbon that exist in soil cores. Using Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) on microcosm samples from early phase litter decomposition, we found that protein- and tannin-like compounds exhibited the strongest correlation to dissolved organic carbon (DOC) concentration. Proteins correlated positively with DOC concentration, while tannins correlated negatively with DOC. Through random forest, neural network, and indicator species analyses, we identified 42 bacterial and 9 fungal taxa associated with DOC concentration. The majority of bacterial taxa (26 out of 42 taxa) belonged to the phylum Proteobacteria while all fungal taxa belonged to the phylum Ascomycota. Additionally, we identified significant connections between microorganisms and protein-like compounds and found that most taxa (12/14) correlated negatively with proteins indicating that microbial consumption of proteins is likely a significant driver of DOC concentration. This research links DOC concentration with microbial production and/or decomposition of specific metabolites to improve our understanding of microbial metabolism and carbon persistence.

Keywords: DOC; FTICR mass spectrometry; bacteria; fungi; metabolites; microbial communities.