Wildfire impacts on soil organic matter biodegradability, metabolomics, and biogeochemical carbon cycling

Abstract

Wildfires are natural ecosystem disturbances that are beneficial to adapted environments. However, global wildfire activity has deviated from historical patterns primarily due to urban expansion into wildland areas, forest management strategies, and climate change. Wildfires are now more intense and frequent, burning larger areas across Earth and impacting air, water, and soil quality. Wildfires impact soil quality by changing the composition of soil organic matter (SOM): a heterogenous mixture of organic molecules in soil ranging from small metabolites to larger lignin-like compounds that comprises two-thirds of Earth's terrestrial carbon stores. SOM serves as critical sustenance supporting soil microbial metabolism and activity, especially SOM that is more biodegradable (i.e. the SOM can be physically accessed, metabolized, and mineralized to CO2 by soil microbes). A key component of biodegradable SOM is the soil metabolome: the assemblage of soil metabolites (e.g. amino acids, organic acids, peptides and saccharides) that drive microbial protein production, cellular energy generation, and soil nutrient cycling. Thus, SOM biodegradability and soil metabolites influence soil carbon cycling and contribute to a healthy, productive soil system. However, the impacts of wildfires on SOM biodegradability and soil metabolite content are largely unknown. Alterations to SOM biodegradability and metabolites could impact microbial activity, biogeochemical nutrient cycling, and the propensity for burned soils to act more as carbon sources rather than carbon sinks. Therefore, the work in this dissertation investigated post-fire SOM biodegradability and soil metabolite contents and was driven by the following questions: How do wildfires impact soil metabolomics, and how do abundances of soil metabolites change after fire? Does SOM become more or less biodegradable after wildfires? These questions were answered across experimental scales from laboratory to field investigations and by using a comprehensive suite of analytical instrumentation. First, we conducted a controlled soil burning experiment using pyrocosms: steel containers filled with soil over which vegetation is burned to simulate a wildfire. The objectives of this study were to 1) characterize SOM and microbial community composition throughout the first month following fire, 2) identify postfire shifts in the soil metabolome and metabolite abundances, and 3) determine how changes in SOM composition correspond to microbial community structure. Using microbial amplicon (16S/ITS) sequencing and gas chromatography-mass spectrometry, heterotrophic microbes (Actinobacteria, Firmicutes, and Proteobacteria) and specific metabolites (glycine, protocatechuate, citric acid cycle intermediates) were enriched in burned soils, indicating that burned soils can contain a variety of substrates that support microbial metabolism. Molecular formulas assigned by 21 T Fourier transform ion cyclotron resonance mass spectrometry revealed that SOM in burned soil was lower in molecular weight and featured 20 to 43 % more nitrogen-containing molecular formulae than SOM in unburned soil. We also measured higher water extractable organic carbon concentrations and higher CO2 respiration in burned soils, implying that the SOM in burned soils may be more biodegradable than the SOM in unburned soils. The observed enrichment of biodegradable SOM, metabolites, and microbial heterotrophs illustrates the resilience of these soils to severe burning, providing important implications for postfire soil microbial activity and carbon cycling. To further explore the impacts of wildfires on soil metabolites, we conducted a laboratory-based, soil heating experiment with the following overarching objective: evaluate how soil metabolite contents change under varying fire intensities. Soils from a lodgepole pine forest, mixed conifer forest, and spruce-fir forest were heated to 150 °C, 250 °C, and 450 °C, and the metabolite contents of the soils were analyzed with gas chromatography-mass spectrometry and liquid chromatography-mass spectrometry. The metabolite contents drastically changed at each heating temperature, indicating that soils burned by wildfires of different intensity conditions will feature disparate metabolite assemblages. Soils heated to 150 °C were enriched in amino acids and peptides while soils heated to 250 °C were enriched in aromatic metabolites, organic acids, and nitrogen-containing saccharides. Surprisingly, 43 to 52 % of the detected metabolites across the three forested ecosystems were significantly more abundant in the heated soils compared to the control soils. These results indicate that soils burned by wildfires (especially of lower intensity) may feature an enriched metabolite pool that could provide essential nutrients for post-fire microbial activity. Lastly, we conducted a field study to determine if our laboratory- and controlled burned-based results were observed in soil burned by an actual wildfire and to address the following objectives: 1) evaluate what metabolites are enriched in burned soil and if SOM is more biodegradable in burned soil from a natural wildfire, 2) determine how differences in soil metabolites and SOM biodegradability may influence short-term soil carbon mineralization and soil CO2 respiration, and 3) assess whether burned soils act more as carbon sinks or carbon sources. We sampled soil from unburned, low severity, and high severity areas from a 2024 Colorado wildfire ~1.5 months post-fire. Ninety-six percent of the putatively identified metabolites were either statistically similar or significantly greater in abundance in burned soils compared to unburned soils. Biological oxygen demand incubations and soil CO2 flux measurements exhibited on average 2.0 to 2.6x greater microbial metabolism of SOM and 1.4 to 2.5x greater CO2 fluxes, respectively, from burned soils relative to unburned soils, suggesting that SOM from burned soil is more biodegradable than from unburned soil. This heightened SOM biodegradability could cause greater microbial metabolism and CO2 emissions from wildfire-impacted soil, potentially shifting post-fire environments from being carbon sinks to carbon sources. Overall, this dissertation used a variety of experimental approaches and instrumentation to discover that burned soils can be enriched in metabolites, SOM from burned soils can be more biodegradable than corresponding unburned soils, and burned soils may act as carbon sources immediately after fire due to this metabolite enrichment and biodegradability enhancement. These results shift our understanding of post-fire SOM composition, and our conceptual understanding of SOM from burned soils should now include a highly reactive pool comprised of enriched metabolites and more biodegradable SOM. This increased biodegradable SOM content could cause post-fire soils to act more like carbon sources, potentially intensifying both climate change and wildfire activity.