Biochar-induced Root Exudates Rewire the Rhizosphere Microbiome and Its Functionality

Biochar amendment has multifaceted benefits on the soil-plant system; yet the underlying mechanisms remain poorly understood. Integrating microfluidics and multi-omics and using wheat as a model plant, we demonstrate that biochar induces differential root exudation which rewires the rhizosphere microbiome and its functionality. Complex molecules in biochar-induced root exudates, particularly plant secondary metabolites and phytohormones, evoke a plant-beneficial rhizosphere microbiome centered by diverse plant growth promoting rhizobacteria (PGPR). Functionally, the restructured microbiome exhibits shifted nitrogen metabolism, characterized by enhanced nitrogen fixation and complete denitrification with reduced N2O emission potential. Additionally, biochar suppresses methane production through orchestrated microbial community functional shifts, including stimulated methionine salvage that deprives the methanogenesis precursor methanethiol; suppressed biosynthesis of coenzyme M, a cofactor required for the methane-forming step; and an enrichment of methanotrophs and thus enhanced methane oxidation. The restructured microbiome also contributes to the transformation of phytohormones and biosynthesis of redox-active quinone compounds, having profound impact on the soil-plant system. Together, our work provides new insights into biochars multifaceted roles in reprogramming the rhizosphere and highlights the promise of engineering the rhizosphere through reshaping root-microbe interactions using designed biochar or root exudate cocktails. Given the fact that fire-derived black carbon shares similar chemistry with biochar and that increased frequency of wildfire could cause more black carbon deposition, this research also spotlights the overlooked impact of fire-derived black carbon on belowground carbon and nitrogen dynamics through intricate rhizosphere interactions. New mechanisms unveiled in this research have implications for both sustainable agriculture and general soil biogeochemistry.