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

Transformations of Soil Organic Carbon Influenced by Volatile Organic Compounds

Authors:

Elizabeth Lunny2* (lunny@aerodyne.com), Zhaoxin Zhang1* (zhaoxinzhang@arizona.edu), Juliana Gil-Loaiza1, Gemma Purser1, Annie DiGuiseppe3, Adrian Castro1, Fangzhou Guo2, Megan Claflin2, Qunli Shen1, Kolby Jardine3, Romy Chakraborty3, Eoin Brodie3, Joanne Shorter3, Joseph R. Roscioli2, Malak M. Tfaily1, Laura Meredith1

Institutions:

1University of Arizona; 2Aerodyne Research, Inc.; 3Lawrence Berkeley National Laboratory

Goals

Volatile organic compounds (VOCs) are ubiquitous carbon (C) pools in the Earth system, but often remain uncharacterized as vectors of soil organic C (SOC) transformations. Roots, litter, aboveground vegetation, and microbial metabolism are all sources of VOCs. However, little is known about how these omnipresent metabolites can contribute to C cycling in soils. This project aims to verify and quantify the direct contributions of VOCs to soil C pools and determine their underpinning ecological and metabolic mechanisms. Moreover, it aims to understand how VOCs connect distant metabolic and biochemical regions through their high mobility in soil. The long-term motivation for this project is to transform the current conceptual understanding and predictive capacity of microbial systems and soil C stabilization to include the important roles of volatile compounds.

Abstract

Volatile organic compounds (VOCs) are diverse and prevalent metabolites exchanged in microbial systems but are often overlooked as vectors of SOC transformations (Honeker et al. 2021; Meredith et al. 2022; Meredith et al. 2023). Roots, litter, aboveground vegetation, and microbial metabolism (Honeker et al. 2023) are all sources of VOCs to soil; however, little is known about how they can contribute to soil C cycling. Microbial uptake of VOCs by soil is increasingly recognized as a ubiquitous process, largely unconstrained by observations. VOCs can contribute to key soil C pools including microbial biomass, dissolved organic matter, particulate organic matter, and mineral-associated organic matter (MAOM), suggesting that they can participate in critical soil C stabilization pathways such as the microbial necromass conduits to MAOM. Yet, understanding is still lacking regarding the fate of VOCs entering the soil system and the specific VOC-induced transformations they may elicit in SOC, hindering the characterization of this process across soil and volatile compounds. To address this research gap, the research team designed complementary studies to evaluate (1) the fate of VOCs added to soil and (2) the contributions of these VOCs to SOC pools in soil from a semi-arid agroecosystem.

In the first experiment, commonly observed VOCs were added into the subsurface of soil columns (100 cm depth) and the concentrations of added VOCs and their gas-phase degradation products were monitored using subsurface gas sampling probes (Roscioli et al. 2021; Gil-Loaiza et al. 2022) at different distances (7 points) from the source. Results indicated that all VOCs were consumed by soil, with the net consumption rates of many increasing over time, indicating microbial acclimation to increased substrate availability or sorption interactions. Interestingly, certain VOCs exhibited greater mobility in the soil compared to others, evidenced by their ability to diffuse over longer distances. This discrepancy in mobility highlights the diverse potential of VOCs to influence SOC levels in adjacent regions, potentially establishing VOC teleconnections within the soil environment.

Finally, partially oxidized volatile products of microbial VOC consumption pathways were observed, revealing the presence of microbes capable of oxidizing isopropanol and acetone.

The second experiment involved a soil incubation study to evaluate the contributions of VOCs to SOC pools using a subset of the compounds tested above. The research team evaluated whether the diversity and quality of SOC changed in response to weekly additions of five individual VOCs over a 3-month period: methanol, acetone, acetaldehyde, isoprene, and ɑ-pinene. Carbon dioxide concentrations were monitored regularly as a proxy for microbial activity. High-resolution SOC analysis by Fourier-transform ion cyclotron resonance mass spectrometry (FTICRMS) revealed that the different VOCs facilitated unique SOC transformations through microbial as well as potentially abiotic processes. Specifically, pinene, methanol, and acetaldehyde drove changes in lipid-like compounds, which represent SOM composition, possibly due to microbial biomass or metabolic pathway activation. External VOC exposure is presumed to have had a priming effect that trained the indigenous microbes to assimilate subsequent VOCs. This study aims to grow understanding of the role of VOCs in soil C cycling and their contributions to soil ecological and metabolic interactions related to C stabilization.

References

Gil-Loaiza, J., et al. 2022. “Versatile Soil Gas Concentration and Isotope Monitoring: Optimization and Integration of Novel Soil Gas Probes with Online Trace Gas Detection,” Biogeosciences 19(1), 165–85.

Honeker L. K., et al. 2021. “The Volatilome: A Vital Piece of the Complete Soil Metabolome,” Frontiers in Environmental Science 9:649905.

Honeker, L., et al. 2023. “Soil Emissions of Three Volatile Metabolites Induced by Drought in an Artificial Tropical Rainforest,” Nature Microbiology 8, 1480–94. DOI:10.1038/s41564-023-01432-9.

Meredith, L. K., and M. M. Tfaily. 2022. “Capturing the Microbial Volatilome: an Often Overlooked ‘Ome’,” Trends in Microbiology 30,(7), 622–31.

Meredith, L. K., et al. 2023. “Automating Methods for Estimating Metabolite Volatility,” Frontiers in Microbiology 14, 1267234. DOI:10.3389/fmicb.2023.1267234.

Roscioli, J. R., et al. 2021. “Soil Gas Probes for Monitoring Trace Gas Messengers of Microbial Activity,” Scientific Reports 11(1), 8327.

Funding Information

This material is based upon work supported by the DOE Office of Science, BER Program, under the following programs: (1) GSP under contract number DE-SC0023189 to the University of Arizona; (2) Small Business Innovation Research Program under contract number DE-SC0018459 to Aerodyne Research, Inc.; and (3) Environmental Research Environmental System Science Program under contract number DE-AC02-05CH11231 to Lawrence Berkeley National Laboratory. This material is also based upon work supported by the NSF Signals in the Soil program under grant no. 2034192 to the University of Arizona.