Chaparral wildfire shifts the functional potential for soil pyrogenic organic matter and nitrogen cycling

Abstract

Wildfires reshape soil microbiomes and chemistry, enhancing nitrogen availability and leaving behind pyrogenic organic matter (PyOM), a difficult to degrade carbon substrate potentially used by pyrophilous or "fire-loving" microbes. Understanding whether pyrophilous bacteria can metabolize post-fire resources is critical for predicting the fate of both carbon and nitrogen. We explored how secondary succession of pyrophilous bacteria align with changes in functional gene composition, particularly genes related to PyOM degradation and microbial nitrogen metabolism using shotgun metagenomics on 30 burned and unburned soils collected at 17, 25, 34, 131, and 376 days after a high-severity wildfire in a fire-adapted chaparral in Southern California. In burned soils, genes for PyOM degradation increased over time by 167% and for inorganic nitrogen cycling by 117%, while unburned soils showed no significant changes. Genes encoding catechol and protocatechuate, intermediates in the PyOM degradation pathway, indicate that the easier-to-degrade ortho-cleavage pathways consistently dominated the burned plots. These pathways co-occurred with genes for nitrification and nitrogen retention, including assimilatory and dissimilatory nitrate reduction to ammonia (DNRA). We also identified 446 bacterial metagenome-assembled genomes (MAGs) and linked gene profiles to dominant taxa and found that increases in genes for PyOM and nitrogen cycling paralleled the dominance of pyrophilous Massilia and Noviherbaspirillum, which encoded distinct pathways for PyOM and inorganic nitrogen use over time. Together, these findings reveal previously unrecognized functional shifts in bacterial communities over a high-resolution successional timeline, providing insights into the long-term impact of fire on microbial-mediated ecosystem processes that shape soil carbon and nitrogen dynamics.