Agroforestry promotes time-dependent recovery of microbial functional diversity and carbon cycling in degraded pasture Amazonian soils

Amazon deforestation is approaching a critical tipping point, threatening ecosystem services and highlighting the need for more sustainable land-use systems. Agroforestry promotes sustainability through soil microorganisms that drive organic matter turnover and nutrient cycling. Understanding the links between microbial functions and soil organic matter is therefore essential for improving ecosystem resilience. We hypothesized that microbial genes related to carbon degradation are associated with dissolved organic matter (DOM) composition in agroforests. We evaluated a chronosequence of agroforests (10, 20, and 30 years-old) using pasture and primary forest as references. By integrating shotgun metagenomics with high-resolution mass spectrometry, we examined microbial and DOM composition interactions. We observed that microbial composition variability was 30% explained by soil chemistry, while DOM composition was 28% explained by land-use type. Agroforests soils showed higher consumption of sucrose and α-glucan, and greater abundance (~43%) of aliphatic DOM, indicating increased presence of microbial-derived compounds. The 30-year agroforest was enriched in genes for recalcitrant carbon degradation (lignin and peptidoglycan), resembling primary forests. Conversely, the 10-year agroforest showed higher abundance of genes (GH36, GH5 and CE3) associated with cellulose and hemicellulose degradation, similar to pastures. Bacterial and fungal α and β-diversity reflected this trend, with higher Pseudomonodata abundance in agroforests versus Actinomycetota in pasture. Soil pH primarily drove microbial-derived compound degradation, while available phosphorus mainly influenced plant-derived compound degradation. Our results indicate agroforests progressively shift from chemical- to microbially-driven carbon cycling, while DOM remains dynamic, reflecting vegetation and seasonal changes, with potential for long-term soil carbon stabilization and soil health.