Arms Race in Evolution of Metabolic Diversity

Within a few years after new chemicals, pesticides or antibiotics enter the biosphere, pathways evolve to allow the compounds to support growth of bacteria. Often the chemicals must be modified to make them less susceptible to biodegradation if they are to remain effective. There seems to be a similar arms race in natural ecosystems among the organisms that engage in chemical communication and defense. Plants produce allelopathic chemicals to suppress competing species or pathogens. Once bacteria evolve the ability to degrade such chemicals their effectiveness would be reduced. Allelopathic plants often produce multiple analogs of the active chemicals which suggests the operation of an arms race among the plants, the target species and the bacteria. Stilbenes such as resveratrol are antifungal compounds produced by a variety of plants including peanuts and grapes. In peanuts resveratrol is accompanied by up to 20 different homologs. We found that resveratrol is readily biodegraded by a diverse community of bacteria in the rhizosphere. The initial attack is catalyzed by an oxygenase closely related to carotenoid cleavage oxygenases including lignostilbene dioxygenase. The initial enzyme has very limited activity toward the most common homologs of resveratrol which suggests they are more recently evolved and less susceptible to biodegradation. Such an arms race could account for many of the myriad small organic compounds produced in the biosphere. Understanding the ecological roles of bacterial catabolic pathways could provide the basis for interventions to limit the spread of invasive plants or improve the defenses of agriculturally important crops.