Genetic memory devices to detect specialized metabolites in plant and soil microbiomes

Root-associated microbiomes significantly influence plant growth and resilience through intricate chemical dialogues mediated by plant- and microbe-derived specialized metabolites. These metabolites play pivotal roles in shaping the assembly, dynamics, and ecological functions of soil microbiomes. Despite advances in in vitro and DNA sequencing studies, a comprehensive understanding of in situ chemical signaling within plant and soil microbiomes remains elusive due to experimental constraints. To address this gap, we developed and tuned a set of five whole-cell biosensors in Escherichia coli for spatiotemporal, non-disruptive detection of biologically relevant specialized metabolites, including 2,4-diacetylphloroglucinol, pyoluteorin, tetracycline, salicylic acid, and naringenin. Four of these biosensors were successfully adapted to the soil-compatible Pseudomonas putida KT2440 Δall-Φ strain, enabling the detection of transient bioavailable signals central to plant-microbe interactions. Additionally, the four sensors were shown to respond to their cognate ligand in a non-sterile soil extract medium containing the diverse microbiome found in soil. By employing genetic memory devices with DNA barcodes for readouts, our approach provides a scalable platform for sensing additional specialized metabolites in the future. This work demonstrates the potential of real-time biosensor technologies to unravel the complex chemical interactions driving soil microbiome ecology, with implications for sustainable agricultural practices.