Long-term ecosystem development and retrogression drive microbial specialization for complex organic matter degradation

Long-term ecosystem development includes a build-up phase followed by a decline (retrogressive) phase characterized by reduced plant productivity and belowground process rates due to reduced nutrient availability. In boreal forests, retrogression is accompanied by soil organic matter (SOM) accumulation, especially in the prolonged absence of fire. However, the role of bacterial communities in SOM dynamics during ecosystem retrogression has been little explored. Using a 5000-year post-fire boreal forest chronosequence, we investigated how long-term succession and retrogression shapes soil bacterial community structure and functional specialization. While the Actinomycetota phylum dominated communities across all chronosequence stages, a significant family-level shift within this phylum occurred in the later (retrogressive) phase, characterized by a transition from Mycobacteriaceae to Streptosporangiaceae. The recovery of metagenome-assembled genomes (MAGs) revealed distinct life-history trade-offs between these families. Streptosporangiaceae MAGs were significantly enriched in genes for degrading phenolics, cellulose, and lignin, and exhibited potential for chitin, lipid and peptide degradation. This positions them as potential decomposers of the primary constituents of stored soil carbon, including plant-derived complex carbohydrates and fungal necromass, during retrogression when fungal activity declines. In contrast, Mycobacteriaceae MAGs are likely to prioritize inorganic phosphate (Pi) uptake-by pstS gene enrichment-, reflecting adaptation to P availability changes during ecosystem development. Collectively, our results demonstrate that long-term ecosystem retrogression drives shifts in the bacterial communities and functions within the Actinomycetota. These shifts may indicate possible divergent strategies, i.e., recalcitrant carbon turnover versus nutrient scavenging, which could explain shifts in the microbial community as the ecosystem transitions toward retrogressive, nutrient-limited states.