The response of the soil and phyllosphere microbial community to repeated application of the fungicide iprodione: Selection for biodegradation or toxicity?

Although pesticide effects on the soil microbial communities have been intensively studied in the late years, little is known about other environments such as the phyllosphere. The mechanisms driving these interactions are well established in soil but not in other pesticides-exposed ecosystems. We tested the hypothesis that soil and phyllosphere microbial communities respond uniformly to the fungicide iprodione. Pepper plants received five repeated (30-d intervals) foliage or soil applications of iprodione. The development of accelerated biodegradation of iprodione was determined via measurement of its presence and transformation in soil and leaves. The response of the soil and epiphytic microbial communities to the regular pesticide exposure was determined via amplicon sequencing. Iprodione-degrading bacteria were isolated from leaves and soil and the transformation pathway was determined via HPLC-PDA. Epiphytic and soil microbial communities responded uniformly to iprodione. Repeated applications led to a gradual acceleration in the degradation of iprodione. Bacterial and Archaeal communities showed little disturbance by iprodione. Whereas the fungal community was significantly altered, especially in soil where Sordariomycetes, Agaricomycetes were stimulated and Dothideomycetes were inhibited. Differential abundance analysis highlighted (a) the stimulation of epiphytic Arthrobacter known as exclusive degraders of iprodione in soil and (b) the inhibition of the soil ammonia-oxidizing Crenarcheon Candidatus Nitososphaera. Enrichment cultures resulted in the isolation of the same iprodione-degrading Paenarthrobacter strain from soil and leaves which hydrolyzed iprodione to 3,5-dichloraniline via the formation of 3,5-dichlorophenyl-carboxiamide and 3,5-dichlorophenylurea-acetate.