Genomic innovation through fragmentation and gene transfer underlies adaptation in pyrophilous bacteria

Abstract

Wildfires reshape soil carbon (C) and nitrogen (N) dynamics by generating pyrogenic organic matter (PyOM) and selecting for pyrophilous "fire-loving" bacteria, yet the genomic mechanisms underpinning their post-fire adaptations are largely unknown. We combined comparative genomics of 16 pyrophilous bacteria spanning three phyla with bioassays and transcriptome profiling following PyOM exposure to test whether post-fire conditions promote genomic innovation within bacterial populations. Pyrophilous bacterial 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 sister taxa. Plasmid-encoded PyOM metabolism genes showed evidence of HGT across pyrophilous bacterial orders and cross-kingdom with pyrophilous fungi. Bioassays revealed overflow organic acid production associated with variation in tricarboxylic acid cycle genes, potentially moderating elevated post-fire soil pH and facilitating microbial succession. Our findings reveal how fire selects for bacterial genomic innovation and illuminate microbial evolution in extreme environments.