Strain-Level Adaptation of Pyrophilous Bacteria through Gene Fragmentation and Horizontal Gene Transfer

Wildfires reshape soil carbon (C) and nitrogen (N) dynamics by generating pyrogenic organic matter (PyOM) and create physicochemical conditions that select for pyrophilous bacteria-yet the genomic basis of their adaptation remains unknown. We combined comparative genomics of 16 pyrophilous bacteria spanning three phyla with bioassays and transcriptome profiling under PyOM amendment to test whether fire-driven conditions promote strain-level genomic innovation. The pyrophilous isolates exhibited genomic novelty through gene fragmentation, horizontal gene transfer (HGT), and plasmid-mediated operon expansion, enriching aromatic C degradation and N acquisition genes relative to non-pyrophilous sisters. Plasmid-encoded PyOM metabolism genes showed evidence of HGT across pyrophilous bacterial orders and even cross-kingdom exchange with fungi. Bioassays revealed overflow organic acid production linked to variation in tricarboxylic acid cycle genes, potentially moderating elevated post-fire soil pH and facilitating microbial succession. These findings reveal how fire selects for genomic innovation in bacteria and illuminate microbial evolution in extreme environments.