Mycofumigation by the Volatile Organic Compound-Producing Fungus Muscodor albus Induces Bacterial Cell Death through DNA Damage

ABSTRACTMuscodor albusbelongs to a genus of endophytic fungi that inhibit and kill other fungi, bacteria, and insects through production of a complex mixture of volatile organic compounds (VOCs). This process of mycofumigation has found commercial application for control of human and plant pathogens, but the mechanism of the VOC toxicity is unknown. Here, the mode of action of these volatiles was investigated through a series of genetic screens and biochemical assays. A single-gene knockout screen revealed high sensitivity forEscherichia colilacking enzymes in the pathways of DNA repair, DNA metabolic process, and response to stress when exposed to the VOCs ofM. albus. Furthermore, the sensitivity of knockouts involved in the repair of specific DNA alkyl adducts suggests that the VOCs may induce alkylation. Evidence of DNA damage suggests that these adducts lead to breaks during DNA replication or transcription if not properly repaired. Additional cytotoxicity profiling indicated that during VOC exposure,E. colibecame filamentous and demonstrated an increase in cellular membrane fluidity. The volatile nature of the toxic compounds produced byM. albusand their broad range of inhibition make this fungus an attractive biological agent. Understanding the antimicrobial effects and the VOC mode of action will inform the utility and safety of potential mycofumigation applications forM. albus.

Effect of biofumigation with volatiles from Muscodor albus on the viability of Tilletia spp. teliospores

Volatile organic compounds produced by the fungus Muscodor albus inhibit or kill numerous fungi. The effect of these volatiles was tested on dormant and physiologically active teliospores of the smut fungi Tilletia horrida , Tilletia indica , and Tilletia tritici , which cause kernel smut of rice, Karnal bunt of wheat, and common bunt of wheat, respectively. Reactivated rye grain culture of M. albus was used to fumigate dormant teliospores in dry Petri dishes and physiologically active teliospores on water agar for up to 5 days at 22 °C. Teliospores of all 3 species were incapable of germination when fumigated on agar for 5 days. When T. tritici on agar was fumigated only during the initial 48 h of incubation, viability was reduced by 73%–99%. Fumigation of dry loose teliospores of T. tritici caused a 69%–97% loss in viability, whereas teliospores within intact sori were not affected. Dormant teliospores of T. horrida and T. indica were not affected by M. albus volatiles. It appears that M. albus has potential as a seed or soil treatment for controlling seedling-infecting smuts where infection is initiated by germinating teliospores prior to seedling emergence. The volatiles were not effective for postharvest control of teliospores under conditions used in these experiments.