Comparative genomic and transcriptomic analysis reveals why Paenarthrobacter strains are specialists in the degradation of the fungicide iprodione. Micrococcaceae

Paenarthrobacter strains effectively degrade the fungicide iprodione, exhibiting aspecialization rarely seen amongst bacteria. The transformation of iprodione iscontrolled by an amidase, a deacetylase and a hydrolase encoded by ipaH, ddaH andduaH respectively. We aimed to elucidate the mechanisms of this catabolicspecialization and its evolution in Paenarthrobacters. The genomes of two newiprodione-degrading Paenarthrobacter strains TA1.8 and C1 were sequenced andanalyzed comparatively with the genomes of two other iprodione-degradingPaenarthrobacter strains YJN-5 and YJN-D. Comparative genomics revealeddifferent gene organization motifs amongst strains which suggest that the strains are atdifferent stages of pathway evolution, in accord with their prior exposure to iprodione.Strains TA1.8, YJN-5 and YJN-D, all isolated from soils heavily exposed toiprodione, carried multiple copies of ipaH, ddaH and duaH in their chromosomes andplasmids that were assigned to two distinct phylogenetic clusters based on genometopology. Conversely, strain C1, isolated from a pristine soil, carried ipaH, ddaH andduaH in the chromosome. Pangenome analysis of the genus Paenarthrobacter placedipaH and duaH in the core genome reinforcing their specialization in the degradationof iprodione as they need to acquire only ddaH, the sole gene of the pathwayassociated with transposable elements in strains C1 and TA1.8, to complete thepathway. We propose an evolution route of the iprodione transformation pathwaywhich involves acquisition of ddaH through horizontal gene transfer, gene duplicationof the chromosomally encoded ipaH and ddaH, and further genetic rearrangementsfor pathway optimization, complementing duaH, a core gene in Paenarthrobacters.Transcriptomic analysis of strain TA1.8 verified the involvement of all copies ofipaH, ddaH and duaH in the transformation of iprodione, and identifiedhydantoinases, upregulated during iprodione degradation, as potential facilitators ofthe transformation of the hydantoin-containing intermediate N-(3,-5-dichlorophenyl)-2,4-dioxoimida-zolidine, a step mediated by DdaH.