Abstract
Biochar can enhance soil health and plant productivity, but the underlying mechanisms remain elusive. Here we tackled this question through the lens of the rhizosphere using wheat as a model plant. We examined the impact of four feedstocks (corn stover, cattle manure, pine sawdust, or wheat straw) and two application rates. Biochar modulated root metabolism, where amino acid metabolism was the most common, leading to cascade effects on a wide range of secondary metabolites, including many plant signaling molecules involved in plant–microbe interactions. All biochar treatments increased rhizosphere microbial diversity, altered community composition, enhanced microbial interactions, and resulted in potential functional changes. Increased Burkholderiales (denitrifying bacteria) abundance and decreased Thermoplasmata (archaeal methanogens) abundance could explain biochar’s widely reported effects of mitigating nitrous oxide and methane. Biochar enhanced positive correlations among microbes and network modularity, suggesting local adaptation through synergism and the formation of modules of functionally interrelated taxa. A diversity of keystone taxa from dominant and non-dominant phyla emerged, including those known to mediate methane, nitrogen, and sulfur cycling. Treatment-specific alterations also occurred, and biochar feedstock choice exerted greater influence than application rate. Wheat biochar at 0.25% showed the strongest and distinct modulating effects, resulting in orchestrated changes in root metabolome and rhizosphere microbiome, especially those relevant to plant–microbe interactions and plant growth promotion. Our work provides new insights into the potential of top-down rhizosphere microbiome engineering through biochar-based reprogramming of root-microbe interactions.