Comparative Genomic and Transcriptomic Analysis Reveals Why <i>Paenarthrobacter</i> Strains Are Specialists in the Degradation of the Fungicide Iprodione

Paenarthrobacters degrade the fungicide iprodione through a pathway involving an amidase (IpaH), a deacetylase (DdaH) and a hydrolase (DuaH). We aimed to elucidate the mechanisms of this catabolic specialisation and its evolution in Paenarthrobacters. Two new iprodione-degrading Paenarthrobacter strains TA1.8 and C1 were sequenced, and their genomes were analysed comparatively to the iprodione-degrading Paenarthrobacter strains YJN-5 and YJN-D. We noted different gene organisation motifs amongst strains, suggesting different stages of pathway evolution in the studied strains depending on their prior exposure to iprodione. Strains derived from soils exposed to iprodione (TA1.8, YJN-5 and YJN-D) carry multiple copies of ipaH, ddaH and duaH. Conversely, strain C1, isolated from a pristine soil, carried one copy of the set. Comparative genomics and pangenome analysis of Paenarthrobacters suggested an evolution route of the iprodione transformation pathway which involves acquisition of ddaH through horizontal gene transfer, gene duplication of the chromosomally encoded ipaH and ddaH, and further genetic rearrangements for pathway optimisation, complementing duaH, a core gene in Paenarthrobacters. Transcriptomic analysis of TA1.8 verified the importance of all ipaH, ddaH and duaH homologues in iprodione transformation and pointed to hydantoinases as potential facilitators of the transformation of the hydantoin-containing intermediate N-(3,-5-dichlorophenyl)-2,4-dioxoimida-zolidine, a step mediated by DdaH.