Charcoal Disrupts Soil Microbial Communication through a Combination of Signal Sorption and Hydrolysis

The presence of charcoal in soil triggers a range of biological effects that are not yet predictable, in part because it interferes with the functioning of chemical signals that microbes release into their environment to communicate. We do not fully understand the mechanisms by which charcoal alters the biologically available concentrations of these intercellular signals. Recently, charcoal has been shown to sorb the signaling molecules that microbes release, rendering them ineffective for intercellular communication. Here, we investigate a second, potentially more important mechanism of interference: signaling-molecule hydrolysis driven by charcoal-induced soil pH changes. We examined the effects of 10 charcoals on the bioavailable concentration of an acyl-homoserine lactone (AHL) used by many Gram-negative bacteria for cell-cell communication. We show that charcoals decrease the level of bioavailable AHL through sorption and pH-dependent hydrolysis of the lactone ring. We then built a quantitative model that predicts the half-lives of different microbial signaling compounds in the presence of charcoals varying in pH and surface area. Our model results suggest that the chemical effects of charcoal on pH-sensitive bacterial AHL signals will be fundamentally distinct from effects on pH-insensitive fungal signals, potentially leading to shifts in microbial community structures.